Inhibition of AAK1 kinase as a novel therapeutic approach to treat neuropathic pain

Journal of Pharmacology and Experimental Therapeutics

Volumn 358, Issue 3, 2016, Pages 371-386

  Kostich, Walter ^a   Hamman, Brian D ^f   Li, Yu Wen ^a   Naidu, Sreenivasulu ^a,e   Dandapani, Kumaran ^a,e   Feng, Jianlin ^a   Easton, Amy ^a   Bourin, Clotilde ^a   Baker, Kevin ^f   Allen, Jason ^f   Savelieva, Katerina ^f   Louis, Justin V ^a,e   Dokania, Manoj ^a,e   Elavazhagan, Saravanan ^a,e   Vattikundala, Pradeep ^a,e   Sharma, Vivek ^a,e   Das, Manish Lal ^a,e   Shankar, Ganesh ^a,e   Kumar, Anoop ^a,e   Holenarsipur, Vinay K ^a,e   Gulianello, Michael ^a   Molski, Ted ^a   Brown, Jeffrey M ^a   Lewis, Martin ^a   Huang, Yanling ^a   Lu, Yifeng ^a   Pieschl, Rick ^a   O'malley, Kevin ^a   Lippy, Jonathan ^a   Nouraldeen, Amr ^f   Lanthorn, Thomas H ^f   Ye, Guilan ^f   Wilson, Alan ^f   Balakrishnan, Anand ^c   Denton, Rex ^d   Grace, James E ^c   Lentz, Kimberley A ^c   Santone, Kenneth S ^c   Bi, Yingzhi ^f   Main, Alan ^f   Swaffield, Jon ^e   Carson, Ken ^f   Mandlekar, Sandhya ^a,e   Vikramadithyan, Reeba K ^a,e   Nara, Susheel J ^a,e   Dzierba, Carolyn ^b   Bronson, Joanne ^b   Macor, John E ^b   Zaczek, Robert ^a   Westphal, Ryan ^a   Kiss, Laszlo ^a   Bristow, Linda ^a   Conway, Charles M ^a   Zambrowicz, Brian ^f,g   Albright, Charles F ^a   more..

^a BRISTOL MYERS SQUIBB   (United States)

^b Neuroscience Chemistry   (United States)

^c Preclinical Candidate Optimization   (United States)

^d Discovery Toxicology   (United States)

^e BMS Research Center   (India)

^f LEXICON PHARMACEUTICALS INC   (United States)

^g REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN 2 ASSOCIATED KINASE 1; LP 935509; PROTEIN SERINE THREONINE KINASE INHIBITOR; STREPTOZOCIN; UNCLASSIFIED DRUG; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEUROPATHIC ACTIVITY; ARTICLE; CHRONIC CONSTRICTION INJURY; DIABETIC NEUROPATHY; DRUG ACTIVITY; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG HALF LIFE; DRUG TISSUE LEVEL; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EMBRYO; ENZYME INHIBITION; ENZYME MECHANISM; EVOKED RESPONSE; FEMALE; FORMALIN TEST; HOT PLATE TEST; LIMIT OF QUANTITATION; MALE; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; RAT; TREATMENT RESPONSE; ANIMAL; ANTAGONISTS AND INHIBITORS; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; GENE INACTIVATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; NEURALGIA; NOCICEPTION; PATHOPHYSIOLOGY; PHENOTYPE; SPINAL CORD;

ANIMALS; ELECTROPHYSIOLOGICAL PHENOMENA; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HUMANS; MALE; MICE; NEURALGIA; NOCICEPTION; PHENOTYPE; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; RATS; SPINAL CORD;

EID: 84983804166     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.116.235333     Document Type: Article

References (56)

1. Arendt-Nielsen L, Mansikka H, Staahl C, Rees H, Tan K, Smart TS, Monhemius R, Suzuki R, and Drewes AM (2011) A translational study of the effects of ketamine and pregabalin on temporal summation of experimental pain. Reg Anesth Pain Med 36:585-591.
2. Beltran del Rio H, Kern F, Lanthorn T, Oravecz T, Piggott J, Powell D, Ramirez-Solis R, Sands AT, and Zambrowicz B (2003) Saturation screening of the druggable mammalian genome, in Model Organisms in Drug Discovery (Carroll P and Fitzgerald K eds) pp 251-278, Wiley & Sons, Chichester, UK.
3. Benarroch EE (2008) Descending monoaminergic pain modulation: bidirectional control and clinical relevance. Neurology 71:217-221.
4. Bennett GJ and Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107.
5. Brommage R, Desai U, Revelli JP, Donoviel DB, Fontenot GK, Dacosta CM, Smith DD, Kirkpatrick LL, Coker KJ, and Donoviel MS, et al. (2008) High- Throughput screening of mouse knockout lines identifies true lean and obese phenotypes. Obesity 16:2362-2367.
6. Brommage R, Liu J, Hansen GM, Kirkpatrick LL, Potter DG, Sands AT, Zambrowicz B, Powell DR, and Vogel P (2014) High- Throughput screening of mouse gene knockouts identifies established and novel skeletal phenotypes. Bone Res 2:14034.
7. Chaplan SR, Bach FW, Pogrel JW, Chung JM, and Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
8. Chaumont S, André C, Perrais D, Boué-Grabot E, Taly A, and Garret M (2013) Agonist-dependent endocytosis of g- Aminobutyric acid type A (GABAA) receptors revealed by a g2(R43Q) epilepsy mutation. J Biol Chem 288:28254-28265.
9. Conner SD and Schmid SL (2002) Identification of an adaptor- Associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J Cell Biol 156:921-929.
10. Costigan M, Scholz J, and Woolf CJ (2009) Neuropathic pain: A maladaptive response of the nervous system to damage. Annu Rev Neurosci 32:1-32.
11. Courteix C, Eschalier A, and Lavarenne J (1993) Streptozocin-induced diabetic rats: behavioural evidence for a model of chronic pain. Pain 53:81-88.
12. D'Amour FE and Smith DL (1941) A method for determining loss of pain sensation. J Pharmacol Exp Ther 72:74-79.
13. Dolphin AC (2012) Calcium channel auxiliary a2d and b subunits: Trafficking and one step beyond. Nat Rev Neurosci 13:542-555.
14. Dubuisson D and Dennis SG (1977) The formalin test: A quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 4:161-174.
15. Dunham NW and Miya TS (1957) A note on a simple apparatus for detecting neurological deficit in rats and mice. J Am Pharm Assoc Am Pharm Assoc 46:208-209.
16. Engelman E and Marsala C (2013) Efficacy of adding clonidine to intrathecal morphine in acute postoperative pain: meta- Analysis. Br J Anaesth 110:21-27.
17. Fairbanks CA (2003) Spinal delivery of analgesics in experimental models of pain and analgesia. Adv Drug Deliv Rev 55:1007-1041.
18. Fairbanks CA, Stone LS, and Wilcox GL (2009) Pharmacological profiles of alpha 2 adrenergic receptor agonists identified using genetically altered mice and isobolographic analysis. Pharmacol Ther 123:224-238.
19. Fields H (2004) State-dependent opioid control of pain. Nat Rev Neurosci 5:565-575.
20. Finnerup NB, Sindrup SH, and Jensen TS (2010) The evidence for pharmacological treatment of neuropathic pain. Pain 150:573-581.
21. Gupta-Rossi N, Ortica S, Meas-Yedid V, Heuss S, Moretti J, Olivo-Marin JC, and Israël A (2011) The adaptor- Associated kinase 1, AAK1, is a positive regulator of the Notch pathway. J Biol Chem 286:18720-18730.
22. Hargreaves K, Dubner R, Brown F, Flores C, and Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
23. Hayashida K, Obata H, Nakajima K, and Eisenach JC (2008) Gabapentin acts within the locus coeruleus to alleviate neuropathic pain. Anesthesiology 109:1077-1084.
24. Hayashida K, Parker R, and Eisenach JC (2007) Oral gabapentin activates spinal cholinergic circuits to reduce hypersensitivity after peripheral nerve injury and interacts synergistically with oral donepezil. Anesthesiology 106:1213-1219.
25. Hylden JL and Wilcox GL (1980) Intrathecal morphine in mice: A new technique. Eur J Pharmacol 67:313-316.
26. Jackson AP, Flett A, Smythe C, Hufton L, Wettey FR, and Smythe E (2003) Clathrin promotes incorporation of cargo into coated pits by activation of the AP2 adaptor micro2 kinase. J Cell Biol 163:231-236.
27. Kearns AE, Donohue MM, Sanyal B, and Demay MB (2001) Cloning and characterization of a novel protein kinase that impairs osteoblast differentiation in vitro. J Biol Chem 276:42213-42218.
28. Kim SH and Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363.
29. Kittler JT, Chen G, Kukhtina V, Vahedi-Faridi A, Gu Z, Tretter V, Smith KR, McAinsh K, Arancibia-Carcamo IL, and Saenger W, et al. (2008) Regulation of synaptic inhibition by phospho-dependent binding of the AP2 complex to a YECL motif in the GABAA receptor gamma2 subunit. Proc Natl Acad Sci USA 105: 3616-3621.
30. Kuai L, Ong SE, Madison JM, Wang X, Duvall JR, Lewis TA, Luce CJ, Conner SD, Pearlman DA, and Wood JL, et al. (2011) AAK1 identified as an inhibitor of neuregulin-1/ErbB4-dependent neurotrophic factor signaling using integrative chemical genomics and proteomics. Chem Biol 18:891-906.
31. Laird JM and Bennett GJ (1993) An electrophysiological study of dorsal horn neurons in the spinal cord of rats with an experimental peripheral neuropathy. J Neurophysiol 69:2072-2085.
32. Liu C and Walker JM (2006) Effects of a cannabinoid agonist on spinal nociceptive neurons in a rodent model of neuropathic pain. J Neurophysiol 96:2984-2994.
33. McCarson KE and Enna SJ (2014) GABA pharmacology: The search for analgesics. Neurochem Res 39:1948-1963.
34. Mestre C, Pélissier T, Fialip J, Wilcox G, and Eschalier A (1994) A method to perform direct transcutaneous intrathecal injection in rats. J Pharmacol Toxicol Methods 32:197-200.
35. Mogil JS (2009) Animal models of pain: progress and challenges. Nat Rev Neurosci 10:283-294.
36. Montana MC, Conrardy BA, Cavallone LF, Kolber BJ, Rao LK, Greco SC, and Gereau RW 4th (2011) Metabotropic glutamate receptor 5 antagonism with fenobam: Examination of analgesic tolerance and side effect profile in mice. Anesthesiology 115: 1239-1250.
37. Morrow TJ (2004) Animal models of painful diabetic neuropathy: The STZ rat model. Curr Protoc Neurosci Chapter 9:Unit 9.18.
38. Obata H, Saito S, Koizuka S, Nishikawa K, and Goto F (2005) The monoaminemediated antiallodynic effects of intrathecally administered milnacipran, a serotonin noradrenaline reuptake inhibitor, in a rat model of neuropathic pain. Anesth Analg 100:1406-1410, table of contents.
39. Powell DR, DaCosta CM, Gay J, Ding ZM, Smith M, Greer J, Doree D, Jeter-Jones S, Mseeh F, and Rodriguez LA, et al. (2013) Improved glycemic control in mice lacking Sglt1 and Sglt2. Am J Physiol Endocrinol Metab 304:E117-E130.
40. Santos-Nogueira E, Redondo Castro E, Mancuso R, and Navarro X (2012) Randall- Selitto test: A new approach for the detection of neuropathic pain after spinal cord injury. J Neurotrauma 29:898-904.
41. Shi B, Conner SD, and Liu J (2014) Dysfunction of endocytic kinase AAK1 in ALS. Int J Mol Sci 15:22918-22932.
42. Snedecor SJ, Sudharshan L, Cappelleri JC, Sadosky A, Desai P, Jalundhwala Y, and Botteman M (2014) Systematic review and meta- Analysis of pharmacological therapies for pain associated with postherpetic neuralgia and less common neuropathic conditions. Int J Clin Pract 68:900-918.
43. Stone LS, German JP, Kitto KF, Fairbanks CA, and Wilcox GL (2014) Morphine and clonidine combination therapy improves therapeutic window in mice: synergy in antinociceptive but not in sedative or cardiovascular effects. PLoS One 9: E109903.
44. Tang T, Li L, Tang J, Li Y, Lin WY, Martin F, Grant D, Solloway M, Parker L, and Ye W, et al. (2010) A mouse knockout library for secreted and transmembrane proteins. Nat Biotechnol 28:749-755.
45. Tanimoto-Mori S, Nakazato-Imasato E, Toide K, and Kita Y (2008) Pharmacologic investigation of the mechanism underlying cold allodynia using a new cold plate procedure in rats with chronic constriction injuries. Behav Pharmacol 19:85-90.
46. Teasell RW, Mehta S, Aubut JA, Foulon B, Wolfe DL, Hsieh JT, Townson AF, and Short C; Spinal Cord Injury Rehabilitation Evidence Research Team (2010) A systematic review of pharmacologic treatments of pain after spinal cord injury. Arch Phys Med Rehabil 91:816-831.
47. Traub LM (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10:583-596.
48. Ultanir SK, Hertz NT, Li G, Ge WP, Burlingame AL, Pleasure SJ, Shokat KM, Jan LY, and Jan YN (2012) Chemical genetic identification of NDR1/2 kinase substrates AAK1 and Rabin8 uncovers their roles in dendrite arborization and spine development. Neuron 73:1127-1142.
49. Wang G, Dai D, Chen X, Yuan L, Zhang A, Lu Y, and Zhang P (2014) Upregulation of neuregulin-1 reverses signs of neuropathic pain in rats. Int J Clin Exp Pathol 7: 5916-5921.
50. Watzman N, Barry H 3rd, Buckley JP, and Kinnard WJ Jr (1964) Semiautomatic System for Timing Rotarod Performance. J Pharm Sci 53:1429-1430.
51. Woolfe G and MacDonald AD (1944) The evaluation of the analgesic action of pethidine hydrochloride (Demerol). J Pharmacol Exp Ther 80:300-307.
52. Xie K, Qiao F, Sun Y, Wang G, and Hou L (2015) Notch signaling activation is critical to the development of neuropathic pain. BMC Anesthesiol 15:41.
53. Yaksh TL, Ozaki G, McCumber D, Rathbun M, Svensson C, Malkmus S, and Yaksh MC (2001) An automated flinch detecting system for use in the formalin nociceptive bioassay. J Appl Physiol (1985) 90:2386-2402.
54. Ye GL, Savelieva KV, Vogel P, Baker KB, Mason S, Lanthorn TH, and Rajan I (2015) Ligation of mouse L4 and L5 spinal nerves produces robust allodynia without major motor function deficit. Behav Brain Res 276:99-110.
55. Zambrowicz BP and Sands AT (2003) Knockouts model the 100 best-selling drugs: Will they model the next 100? Nat Rev Drug Discov 2:38-51.
56. Zeilhofer HU, Ralvenius WT, and Acuña MA (2015) Restoring the spinal pain gate: GABA(A) receptors as targets for novel analgesics. Adv Pharmacol 73: 71-96.