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Distribution of heme oxygenase-2 and NADPH-diaphorase in the spinal trigeminal nucleus of the rat

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Abstract

Heme oxygenase (HO)/carbon monoxide (CO) and nitric oxide synthase (NOS)/nitric oxide (NO) systems are involved in sensory information processing. The present study was undertaken to examine the distribution of HO-2 and NOS in the spinal trigeminal nucleus (STN) of the rat, using histochemistry and immunohistochemistry. Nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) staining was found that NADPH-d activity was more prominent in the nucleus caudalis (Vc) and the dorsomedial subdivision of the nucleus oralis (Vo) than in other spinal trigeminal regions. Immunohistochemistry for HO-2 revealed that HO-2 staining neurons distributed extensively, which intensity was higher in the rostral than caudal part of the STN. The colocalization of NADPH-d and HO-2 was mainly confined in the Vc. The expression and distribution of NADPH-d and HO-2 suggest that NO and CO are likely neurotransmitters and might function in the processing orofacial signal in the STN together.

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Abbreviations

CNS:

Central nervous system

CO:

Carbon monoxide

DAB:

Diaminobenzidine

DMSp5:

Dorsalmedial spinal trigeminal nucleus

eNOS:

Endothelial NOS

HO:

Heme oxygenase

iNOS:

Inducible NOS

NADPH:

Nicotinamide adenine dinucleotide phosphate

NADPH-d:

NADPH-diaphorase

NBT:

Nitroblue tetrazolium

nNOS:

Neuronal NOS

NO:

Nitric oxide

NOS:

Nitric oxide synthase

STN:

Spinal trigeminal nucleus

Vc:

Nucleus caudalis

Vi:

Nucleus interpolaris

Vo:

Nuleus oralisc

References

  • Baranano DE, Ferris CD, Snyder SH (2001) A typical neural messengers. Trends Neurosci 24:99–106

    Article  CAS  PubMed  Google Scholar 

  • Battish R, Cao GY, Lynn RB et al (2000) Heme oxygenase-2 distribution in anorectum: colocalization with neuronal nitric oxide synthase. Am J Physiol Gastrointest Liver Physiol 278:G148–G155

    CAS  PubMed  Google Scholar 

  • Bredt DS, Snyder SH (1992) Nitric oxide, a novel neuronal messenger. Neuron 8:3–11

    Article  CAS  PubMed  Google Scholar 

  • Dallel R, Raboisson P, Auroy P et al (1988) The rostral part of the trigeminal sensory complex is involved in orofacial nociception. Brain Res 448:7–19

    Article  CAS  PubMed  Google Scholar 

  • Dawson TM, Snyder SH (1994) Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J Neurosci 14:5147–5159

    CAS  PubMed  Google Scholar 

  • Dohrn CS, Mullett MA, Price RH et al (1994) Distribution of nitric oxide synthase–immunoreactive interneurons in the spinal trigeminal nucleus. J Comp Neurol 346:449–460

    Article  CAS  PubMed  Google Scholar 

  • Falls WM, Moore BJ, Schneider MT (1990) Fine structural characteristics and synaptic connections of trigeminocerebellar projection neurons in rat trigeminal nucleus oralis. Somatosens Mot Res 7:1–18

    Article  CAS  PubMed  Google Scholar 

  • Fan W, Dong W, Leng S et al (2008) Expression and colocalization of NADPH-diaphorase and heme oxygenase-2 in trigeminal ganglion and mesencephalic trigeminal nucleus of the rat. J Mol Histol 39:427–433

    Article  CAS  PubMed  Google Scholar 

  • Fan W, Huang F, Li C et al (2009) Involvement of NOS/NO in the development of chronic dental inflammatory pain in rats. Brain Res Rev 59:324–332

    Article  CAS  PubMed  Google Scholar 

  • Gobel S (1975) Golgi studies in the substantia gelatinosa neurons in the spinal trigeminal nucleus. J Comp Neurol 162:397–415

    Article  CAS  PubMed  Google Scholar 

  • Hu JW, Sessle BJ (1984) Comparison of responses of cutaneous nociceptive and nonnociceptive brain stem neurons in trigeminal subnucleus caudalis (medullary dorsal horn) and subnucleus oralis to natural and electrical stimulation of tooth pulp. J Neurophysiol 52:39–53

    CAS  PubMed  Google Scholar 

  • Ignarro LJ, Buga GM, Wood KS et al (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84:9265–9269

    Article  CAS  PubMed  Google Scholar 

  • Ingi T, Cheng J, Ronnett GV (1996) Carbon monoxide: an endogenous modulator of the nitric oxide–cyclic GMP signaling system. Neuron 16:835–842

    Article  CAS  PubMed  Google Scholar 

  • Kolesar D, Kolesarova M, Schreiberova A et al (2006) Distribution of NADPH diaphorase-exhibiting primary afferent neurons in the trigeminal ganglion and mesencephalic trigeminal nucleus of the rabbit. Cell Mol Neurobiol 26:1265–1279

    Article  CAS  PubMed  Google Scholar 

  • Li X, Clark JD (2000a) Heme oxygenase type 2 plays a role in formalin-induced nociception. Pain 86:75–80

    Article  CAS  PubMed  Google Scholar 

  • Li X, Clark JD (2000b) The role of heme oxygenase in neuropathic and incisional pain. Anesth Analg 90:677–682

    Article  CAS  PubMed  Google Scholar 

  • Li X, Clark JD (2001) Heme oxygenase inhibitors reduce formalin-induced Fos expression in mouse spinal cord tissue. Neuroscience 105:949–956

    Article  CAS  PubMed  Google Scholar 

  • Maines MD (1997) The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517–554

    Article  CAS  PubMed  Google Scholar 

  • Nascimento CG, Branco LG (2007) Role of the peripheral heme oxygenase-carbon monoxide pathway on the nociceptive response of rats to the formalin test: evidence for a cGMP signaling pathway. Eur J Pharmacol 556:55–61

    Article  CAS  PubMed  Google Scholar 

  • Nathan C, Xie QW (1994) Nitric oxide synthases: roles, tolls, and controls. Cell 78:915–918

    Article  CAS  PubMed  Google Scholar 

  • Olszewski J (1950) On the anatomical and functional organization of the spinal trigeminal nucleus. J Comp Neurol 92:401–413

    Article  CAS  PubMed  Google Scholar 

  • Phelan KD, Falls WM (1989) An analysis of the cyto- and myeloarchitectonic organization of trigeminal nucleus interpolaris in the rat. Somatosens Mot Res 6:333–366

    CAS  PubMed  Google Scholar 

  • Robinson PP, Boissonade FM, Loescher AR et al (2004) Peripheral mechanisms for the initiation of pain following trigeminal nerve injury. J Orofac Pain 18:287–292

    PubMed  Google Scholar 

  • Roche AK, Cook M, Wilcox GL et al (1996) A nitric oxide synthesis inhibitor (L-NAME) reduces licking behavior and Fos-labeling in the spinal cord of rats during formalin-induced inflammation. Pain 66:331–341

    Article  CAS  PubMed  Google Scholar 

  • Rodella L, Rezzani R, Corsetti G et al (2000) Nitric oxide involvement in the trigeminal hyperalgesia in diabetic rats. Brain Res 865:112–115

    Article  CAS  PubMed  Google Scholar 

  • Sessle BJ (2000) Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 11:57–91

    Article  CAS  PubMed  Google Scholar 

  • Takemura M, Tsujio A, Iwase K et al (1998) Central terminals of orofacial primary afferents and NADPH-diaphorase activity in the trigemino-solitary complex of rats. Brain Res 781:77–89

    Article  CAS  PubMed  Google Scholar 

  • Vincent SR, Das S, Maines MD (1994) Brain heme oxygenase isoenzymes and nitric oxide synthase are co-localized in select neurons. Neuroscience 63:223–231

    Article  CAS  PubMed  Google Scholar 

  • Wood J, Garthwaite J (1994) Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacology 33:1235–1244

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Wang R (2005) Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev 57:585–630

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Mabuchi T, Katano T et al (2007) Nitric oxide (NO) serves as a retrograde messenger to activate neuronal NO synthase in the spinal cord via NMDA receptors. Nitric Oxide 17:18–24

    Article  CAS  PubMed  Google Scholar 

  • Xue L, Farrugia G, Miller SM et al (2000) Carbon monoxide and nitric oxide as coneurotransmitters in the enteric nervous system: evidence from genomic deletion of biosynthetic enzymes. Proc Natl Acad Sci USA 97:1851–1855

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto T, Shimoyama N, Mizuguchi T (1993) Nitric oxide synthase inhibitor blocks spinal sensitization induced by formalin injection into the rat paw. Anesth Analg 77:886–890

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki Y, Ren K, Shimada M et al (2008) Modulation of paratrigeminal nociceptive neurons following temporomandibular joint inflammation in rats. Exp Neurol 214:209–218

    Article  PubMed  Google Scholar 

  • Yonehara N, Kudo C, Kamisaki Y (2003) Involvement of NMDA-nitric oxide pathways in the development of tactile hypersensitivity evoked by the loose-ligation of inferior alveolar nerves in rats. Brain Res 963:232–243

    Article  CAS  PubMed  Google Scholar 

  • Zakhary R, Gaine SP, Dinerman JL et al (1996) Heme oxygenase 2: endothelial and neuronal localization and role in endothelium-dependent relaxation. Proc Natl Acad Sci USA 93:795–798

    Article  CAS  PubMed  Google Scholar 

  • Zambuzzi WF, Paiva KB, Batista AC et al. (2009) Immunohistochemical approach reveals involvement of inducible nitric oxide synthase in rat late development. J Mol Histol

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (NO: 30070952; 30472248) and Science and Technology Planning Project of Guangdong Province, China (NO: 2006B35601007).

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Authors and Affiliations

  1. Department of Oral Anatomy and Physiology, Guanghua School of Stomatology, Sun Yat-sen University, 74 Zhongshan Rd 2, 510080, Guangzhou, China

    Wenguo Fan, Fang Huang, Weiguo Dong, Cuixia Li & Hongwen He

  2. Department of Pediatric Dentistry, Guanghua School of Stomatology, Sun Yat-sen University, 510080, Guangzhou, China

    Fang Huang

  3. Dongshan Division, First Affiliated Hospital, Sun Yat-sen University, 510080, Guangzhou, China

    Zhixiong Gao

  4. Institute of Oncology, Affiliated Tumor Hospital of Guangzhou Medical College, 510095, Guangzhou, China

    Xiao Zhu & Dongpei Li

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  1. Wenguo Fan
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  2. Fang Huang
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  3. Weiguo Dong
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  4. Zhixiong Gao
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  5. Cuixia Li
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  7. Dongpei Li
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  8. Hongwen He
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Correspondence to Fang Huang or Hongwen He.

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Fan, W., Huang, F., Dong, W. et al. Distribution of heme oxygenase-2 and NADPH-diaphorase in the spinal trigeminal nucleus of the rat. J Mol Hist 40, 209–215 (2009). https://doi.org/10.1007/s10735-009-9232-3

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  • DOI: https://doi.org/10.1007/s10735-009-9232-3

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