Differential Development of Facial and Hind Paw Allodynia in a Nitroglycerin-Induced Mouse Model of Chronic Migraine: Role of Capsaicin Sensitive Primary Afferents

Biol Pharm Bull. 2018 Feb 1;41(2):172-181. doi: 10.1248/bpb.b17-00589. Epub 2017 Nov 29.

Abstract

Despite the relatively high prevalence of migraine or headache, the pathophysiological mechanisms triggering headache-associated peripheral hypersensitivities, are unknown. Since nitric oxide (NO) is well known as a causative factor in the pathogenesis of migraine or migraine-associated hypersensitivities, a mouse model has been established using systemic administration of the NO donor, nitroglycerin (NTG). Here we tried to investigate the time course development of facial or hindpaw hypersensitivity after repetitive NTG injection. NTG (10 mg/kg) was administrated to mice every other day for nine days. Two hours post-injection, NTG produced acute mechanical and heat hypersensitivity in the hind paws. By contrast, cold allodynia, but not mechanical hypersensitivity, occurred in the facial region. Moreover, this hindpaws mechanical hypersensitivity and the facial cold allodynia was progressive and long-lasting. We subsequently examined whether the depletion of capsaicin-sensitive primary afferents (CSPAs) with resiniferatoxin (RTX, 0.02 mg/kg) altered these peripheral hypersensitivities in NTG-treated mice. RTX pretreatment did not affect the NTG-induced mechanical allodynia in the hind paws nor the cold allodynia in the facial region, but it did inhibit the development of hind paw heat hyperalgesia. Similarly, NTG injection produced significant hindpaw mechanical allodynia or facial cold allodynia, but not heat hyperalgesia in transient receptor potential type V1 (TRPV1) knockout mice. These findings demonstrate that different peripheral hypersensitivities develop in the face versus hindpaw regions in a mouse model of repetitive NTG-induced migraine, and that these hindpaw mechanical hypersensitivity and facial cold allodynia are not mediated by the activation of CSPAs.

Keywords: allodynia; migraine; nitroglycerin; resiniferatoxin; transient receptor potential type V1 (TRPV1).

Publication types

  • Comparative Study

MeSH terms

  • Animals
  • Capsaicin / pharmacology
  • Cold Temperature / adverse effects
  • Diterpenes / toxicity
  • Drug Resistance
  • Facial Nerve Diseases / chemically induced
  • Facial Nerve Diseases / metabolism
  • Facial Nerve Diseases / pathology
  • Facial Nerve Diseases / physiopathology*
  • Hindlimb
  • Hot Temperature / adverse effects
  • Hyperalgesia / chemically induced
  • Hyperalgesia / metabolism
  • Hyperalgesia / pathology
  • Hyperalgesia / physiopathology*
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Migraine Disorders / metabolism
  • Migraine Disorders / pathology
  • Migraine Disorders / physiopathology*
  • Nerve Tissue Proteins / agonists
  • Nerve Tissue Proteins / antagonists & inhibitors
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neurons, Afferent / drug effects*
  • Neurons, Afferent / metabolism
  • Neurons, Afferent / pathology
  • Neurotoxins / toxicity
  • Nitric Oxide Donors / toxicity
  • Nitroglycerin / toxicity
  • Organ Specificity
  • Peripheral Nervous System Diseases / chemically induced
  • Peripheral Nervous System Diseases / metabolism
  • Peripheral Nervous System Diseases / pathology
  • Peripheral Nervous System Diseases / physiopathology*
  • Sensory System Agents / pharmacology
  • TRPV Cation Channels / agonists
  • TRPV Cation Channels / antagonists & inhibitors
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism*

Substances

  • Diterpenes
  • Nerve Tissue Proteins
  • Neurotoxins
  • Nitric Oxide Donors
  • Sensory System Agents
  • TRPV Cation Channels
  • TRPV1 protein, mouse
  • resiniferatoxin
  • Nitroglycerin
  • Capsaicin