Intrathecal substance p-saporin in the dog distribution, safety, and spinal neurokinin-1 receptor ablation

Anesthesiology

Volumn 119, Issue 5, 2013, Pages 1163-1177

  Wiese, Ashley J ^a   Rathbun, Michael ^a   Butt, Mark T ^b   Malkmus, Shelle A ^a   Richter, Philip J ^b   O Sborn, Kent G ^c   Xu, Qinghao ^a   Veesart, Samantha L ^a   Steinauer, Joanne J ^a   Higgins, Denise ^d   Lappi, Douglas A ^d   Russell, Brian ^d   Yaksh, Tony L ^a  

^a MedVet Cincinnati Medical and Cancer Center for Pets   (United States)

^b Campus Veterinary Medicine ^*  (India)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Advanced Targeting Systems   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALGESIC AGENT; NEUROKININ 1 RECEPTOR; SAPORIN; SUBSTANCE P SAPORIN; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANINE MODEL; CELL COUNT; CELL LOSS; CHRONIC PAIN; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG CEREBROSPINAL FLUID LEVEL; DRUG DISTRIBUTION; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG SAFETY; DRUG TISSUE LEVEL; EXPERIMENTAL DOG; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTRATHECAL CATHETER; INTRATHECAL DRUG ADMINISTRATION; LUMBAR SPINAL CORD; MALE; NONHUMAN; PARAPLEGIA; PELVIC GIRDLE; PRIORITY JOURNAL; SPINAL ANESTHESIA; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; SPINAL CORD VENTRAL HORN; TISSUE SECTION;

ANIMALS; BEHAVIOR, ANIMAL; BLOOD PRESSURE; BODY TEMPERATURE; BODY WEIGHT; DOGS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; IN SITU HYBRIDIZATION; INJECTIONS, SPINAL; NEUROKININ-1 RECEPTOR ANTAGONISTS; NEUROLOGIC EXAMINATION; NEUROTOXICITY SYNDROMES; OPHTHALMOSCOPY; PHENOTYPE; RECEPTORS, NEUROKININ-1; RIBOSOME INACTIVATING PROTEINS, TYPE 1; SPINAL CORD; SUBSTANCE P; TISSUE DISTRIBUTION;

EID: 84888245773     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e3182a95164     Document Type: Article

References (52)

1. Nakaya Y, Kaneko T, Shigemoto R, Nakanishi S, Mizuno N: Immunohistochemical localization of substance P receptor in the central nervous system of the adult rat. J Comp Neurol 1994; 347:249-74
2. Dzurik MV, Diedrich A, Black B, Paranjape SY, Raj SR, Byrne DW, Robertson D: Endogenous substance P modulates human cardiovascular regulation at rest and during orthostatic load. J Appl Physiol 2007; 102:2092-7
3. Nattie EE, Li A: Substance P-saporin lesion of neurons with NK1 receptors in one chemoreceptor site in rats decreases ventilation and chemosensitivity. J Physiol 2002; 544(Pt 2):603-16
4. McLeod AL, Krause JR, Cuello AC, Ribeiro-Da Silva A: Preferential synaptic relationships between substance P immunoreactive boutons and neurokinin 1 receptor sites in the rat. Proc Natl Acad Sci USA 1998; 95:15775-80
5. Todd AJ, Puskar Z, Spike RC, Hughes C, Watt C, Forrest L: Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. J Neurosci 2002; 22:4103-13
6. Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, Daughters RS, Lappi DA, Wiley RG, Simone DA: Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 1997; 278:275-9
7. Polgár E, Al Ghamdi KS, Todd AJ: Two populations of neurokinin 1 receptor-expressing projection neurons in lamina I of the rat spinal cord that differ in AMPA receptor subunit composition and density of excitatory synaptic input. Neuroscience 2010; 167:1192-204
8. Yamamoto T, Yaksh TL: Effects of intrathecal capsaicin and an NK-1 antagonist, CP,96-345, on the thermal hyperalgesia observed following unilateral constriction of the sciatic nerve in the rat. Pain 1992; 51:329-34
9. Parenti C, Aricò G, Ronsisvalle G, Scoto GM: Supraspinal injection of Substance P attenuates allodynia and hyperalgesia in a rat model of inflammatory pain. Peptides 2012; 34:412-8
10. Dionne RA, Max MB, Gordon SM, Parada S, Sang C, Gracely RH, Sethna NF, MacLean DB: The substance P receptor antagonist CP-99,994 reduces acute postoperative pain. Clin Pharmacol Ther 1998; 64:562-8
11. Alvillar BM, Boscan P, Mama KR, Ferreira TH, Congdon J, Twedt DC: Effect of epidural and intravenous use of the neurokinin-1 (NK-1) receptor antagonist maropitant on the sevoflurane minimum alveolar concentration (MAC) in dogs. Vet Anaesth Analg 2012; 39:201-5
12. Boscan P, Monnet E, Mama K, Twedt DC, Congdon J, Steffey EP: Effect of maropitant, a neurokinin 1 receptor antagonist, on anesthetic requirements during noxious visceral stimulation of the ovary in dogs. Am J Vet Res 2011; 72:1576-9
13. Sindrup SH, Graf A, Sfikas N: The NK1-receptor antagonist TKA731 in painful diabetic neuropathy: A randomised, controlled trial. Eur J Pain 2006; 10:567-71
14. Beresford IJ, Birch PJ, Hagan RM, Ireland SJ: Investigation into species variants in tachykinin NK1 receptors by use of the non-peptide antagonist, CP-96,345. Br J Pharmacol 1991; 104:292-3
15. Urban LA, Fox AJ: NK1-r receptor antagonists-Are they really without effect in the pain clinic? Trends Pharmacol Sci 2000; 21:462-4
16. Hill R: NK1 (substance P) receptor antagonists-Why are they not analgesic in humans? Trends Pharmacol Sci 2000; 21:244-6
17. Sluka KA, Westlund KN: Spinal cord amino acid release and content in an arthritis model: The effects of pretreatment with non-NMDA, NMDA, and NK1 receptor antagonists. Brain Res 1993; 627:89-103
18. Almeida TA, Rojo J, Nieto PM, Pinto FM, Hernandez M, Martín JD, Candenas ML: Tachykinins and tachykinin receptors: Structure and activity relationships. Curr Med Chem 2004; 11:2045-81
19. Wiley RG: Substance P receptor-expressing dorsal horn neurons: Lessons from the targeted cytotoxin, substance P-saporin. Pain 2008; 136:7-10
20. Wiley RG, Lappi DA: Targeted toxins in pain. Adv Drug Deliv Rev 2003; 55:1043-54
21. Weng A, Thakur M, von Mallinckrodt B, Beceren-Braun F, Gilabert-Oriol R, Wiesner B, Eichhorst J, Böttger S, Melzig MF, Fuchs H: Saponins modulate the intracellular trafficking of protein toxins. J Control Release 2012; 164:74-86
22. Bolognesi A, Polito L, Scicchitano V, Orrico C, Pasquinelli G, Musiani S, Santi S, Riccio M, Bortolotti M, Battelli MG: Endocytosis and intracellular localisation of type 1 ribosomeinactivating protein saporin-s6. J Biol Regul Homeost Agents 2012; 26:97-109
23. Wiley RG, Lappi DA: Targeting neurokinin-1 receptorexpressing neurons with [Sar9,Met(O2)11 substance P-saporin. Neurosci Lett 1999; 277:1-4
24. Allen JW, Mantyh PW, Horais K, Tozier N, Rogers SD, Ghilardi JR, Cizkova D, Grafe MR, Richter P, Lappi DA, Yaksh TL: Safety evaluation of intrathecal substance P-saporin, a targeted neurotoxin, in dogs. Toxicol Sci 2006; 91:286-98
25. Nichols ML, Allen BJ, Rogers SD, Ghilardi JR, Honore P, Luger NM, Finke MP, Li J, Lappi DA, Simone DA, Mantyh PW: Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 1999; 286:1558-61
26. Khasabov SG, Rogers SD, Ghilardi JR, Peters CM, Mantyh PW, Simone DA: Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 2002; 22:9086-98
27. Choi JI, Koehrn FJ, Sorkin LS: Carrageenan induced phosphorylation of Akt is dependent on neurokinin-1 expressing neurons in the superficial dorsal horn. Mol Pain 2012; 8:4
28. Brown DC, Agnello K: Intrathecal substance P-saporin in the dog: Efficacy in bone cancer pain. Anesthesiology 2013; 119:1178-85
29. Yaksh, TL, Steinauer JJ, Veesart SL, Malkmus SA: Alfentanil: Correlations between absence of effect upon subcutaneous mast cells and absence of granuloma formation after intrathecal infusion in the dog. Neuromodulation 2012; [Epub ahead of print]
30. Hua XY, Yaksh TL: Dorsal Horn Substance P and NK1 Receptors: Study of a Model System in Spinal Nociceptive Processing: Synaptic Plasticity in Pain, 1st edition. New York, Springer, 2009, pp 109-38
31. Abbadie C, Trafton J, Liu H, Mantyh PW, Basbaum AI: Inflammation increases the distribution of dorsal horn neurons that internalize the neurokinin-1 receptor in response to noxious and non-noxious stimulation. J Neurosci 1997; 17:8049-60
32. Honoré P, Kamp EH, Rogers SD, Gebhart GF, Mantyh PW: Activation of lamina I spinal cord neurons that express the substance P receptor in visceral nociception and hyperalgesia. J Pain 2002; 3:3-11
33. Honor P, Menning PM, Rogers SD, Nichols ML, Basbaum AI, Besson JM, Mantyh PW: Spinal substance P receptor expression and internalization in acute, short-term, and long-term inflammatory pain states. J Neurosci 1999; 19:7670-8
34. Bester H, De Felipe C, Hunt SP: The NK1 receptor is essential for the full expression of noxious inhibitory controls in the mouse. J Neurosci 2001; 21:1039-46
35. Li JL, Ding YQ, Xiong KH, Li JS, Shigemoto R, Mizuno N: Substance P receptor (NK1)-immunoreactive neurons projecting to the periaqueductal gray: Distribution in the spinal trigeminal nucleus and the spinal cord of the rat. Neurosci Res 1998; 30:219-25
36. Moussaoui SM, Hermans E, Mathieu AM, Bonici B, Clerc F, Guinet F, Garret C, Laduron PM: Polyclonal antibodies against the rat NK1 receptor: Characterization and localization in the spinal cord. Neuroreport 1992; 3:1073-6
37. McConalogue K, Corvera CU, Gamp PD, Grady EF, Bunnett NW: Desensitization of the neurokinin-1 receptor (NK1-R) in neurons: Effects of substance P on the distribution of NK1-R, Galphaq/11, G-protein receptor kinase-2/3, and beta-arrestin-1/2. Mol Biol Cell 1998; 9:2305-24
38. Shapiro MS, Hille B: Substance P and somatostatin inhibit calcium channels in rat sympathetic neurons via different G protein pathways. Neuron 1993; 10:11-20
39. Ding YQ, Zheng HX, Wang DS, Xu JQ, Gong LW, Lü Y, Qin BZ, Shi J, Li HL, Li JS, Shigemoto R, Kaneko T, Mizuno N: The distribution of substance P receptor (NK1)-like immunoreactive neurons in the newborn and adult human spinal cord. Neurosci Lett 1999; 266:133-6
40. Malmberg AB, Yaksh TL: Hyperalgesia mediated by spinal glutamate or substance P receptor blocked by spinal cyclooxygenase inhibition. Science 1992; 257:1276-9
41. Dirig DM, Yaksh TL: Thermal hyperalgesia in rat evoked by intrathecal substance P at multiple stimulus intensities reflects an increase in the gain of nociceptive processing. Neurosci Lett 1996; 220:93-6
42. Dirig DM, Yaksh TL: In vitro prostanoid release from spinal cord following peripheral inflammation: Effects of substance P, NMDA and capsaicin. Br J Pharmacol 1999; 126:1333-40
43. Ma W, Eisenach JC: Intraplantar injection of a cyclooxygenase inhibitor ketorolac reduces immunoreactivities of substance P, calcitonin gene-related peptide, and dynorphin in the dorsal horn of rats with nerve injury or inflammation. Neuroscience 2003; 121:681-90
44. Ummenhofer WC, Arends RH, Shen DD, Bernards CM: Comparative spinal distribution and clearance kinetics of intrathecally administered morphine, fentanyl, alfentanil, and sufentanil. Anesthesiology 2000; 92:739-53
45. Bernards CM: Cerebrospinal fluid and spinal cord distribution of baclofen and bupivacaine during slow intrathecal infusion in pigs. Anesthesiology 2006; 105:169-78
46. Yaksh TL, Rathbun ML, Dragani JC, Malkmus S, Bourdeau AR, Richter P, Powell H, Myers RR, Lebel CP: Kinetic and safety studies on intrathecally infused recombinant-methionyl human brain-derived neurotrophic factor in dogs. Fundam Appl Toxicol 1997; 38:89-100
47. Yaksh TL, de Kater A, Dean R, Best BM, Miljanich GP: Pharmacokinetic analysis of ziconotide (SNX-111), an intrathecal N-type calcium channel blocking analgesic, delivered by bolus and infusion in the dog. Neuromodulation 2012; 15:508-19; discussion 519
48. Katayama M, Nadel JA, Bunnett NW, Di Maria GU, Haxhiu M, Borson DB: Catabolism of calcitonin gene-related peptide and substance P by neutral endopeptidase. Peptides 1991; 12:563-7
49. Wang LH, Ahmad S, Benter IF, Chow A, Mizutani S, Ward PE: Differential processing of substance P and neurokinin A by plasma dipeptidyl(amino)peptidase IV, aminopeptidase M and angiotensin converting enzyme. Peptides 1991; 12:1357-64
50. Eisenach JC, Shafer SL, Yaksh T: The need for a journal policy on intrathecal, epidural, and perineural administration of non-approved drugs. Pain 2010; 149:417-9
51. Yaksh TL: Spinal delivery and assessment of drug safety, Fundamental Neuropathology for Pathologists and Toxicologists. Principles and Techniques. Edited by Bolon B, Butt MT. Hoboken, John Wiley & Sons, 2011, pp 452-62
52. Walker SM, Yaksh TL: Neuraxial analgesia in neonates and infants: A review of clinical and preclinical strategies for the development of safety and efficacy data. Anesth Analg 2012; 115:638-62