Deletion of Annexin 2 Light Chain P11 in Nociceptors Causes Deficits in Somatosensory Coding and Pain Behavior

Overview

Journal J Neurosci

Specialty Neurology

Date 2006 Oct 13

PMID 17035534

Citations 32

Authors

Thomas Foulkes

Mohammed A Nassar

Tim Lane

Elizabeth A Matthews

Mark D Baker

Volker Gerke

Kenji Okuse

Anthony H Dickenson

John N Wood

Affiliations

Soon will be listed here.

Abstract

The S100 family protein p11 (S100A10, annexin 2 light chain) is involved in the trafficking of the voltage-gated sodium channel Na(V)1.8, TWIK-related acid-sensitive K+ channel (TASK-1), the ligand-gated ion channels acid-sensing ion channel 1a (ASIC1a) and transient receptor potential vanilloid 5/6 (TRPV5/V6), as well as 5-hydroxytryptamine receptor 1B (5-HT1B), a G-protein-coupled receptor. To evaluate the role of p11 in peripheral pain pathways, we generated a loxP-flanked (floxed) p11 mouse and used the Cre-loxP recombinase system to delete p11 exclusively from nociceptive primary sensory neurons in mice. p11-null neurons showed deficits in the expression of Na(V)1.8, but not of annexin 2. Damage-sensing primary neurons from these animals show a reduced tetrodotoxin-resistant sodium current density, consistent with a loss of membrane-associated Na(V)1.8. Noxious coding in wide-dynamic-range neurons in the dorsal horn was markedly compromised. Acute pain behavior was attenuated in certain models, but no deficits in inflammatory pain were observed. A significant deficit in neuropathic pain behavior was also apparent in the conditional-null mice. These results confirm an important role for p11 in nociceptor function.

Citing Articles

Fabry disease Schwann cells release p11 to induce sensory neuron hyperactivity.

Waltz T, Chao D, Prodoehl E, Enders J, Ehlers V, Dharanikota B JCI Insight. 2024; 9(8).

PMID: 38646936 PMC: 11141882. DOI: 10.1172/jci.insight.172869.

Annexins-a family of proteins with distinctive tastes for cell signaling and membrane dynamics.

Gerke V, Gavins F, Geisow M, Grewal T, Jaiswal J, Nylandsted J Nat Commun. 2024; 15(1):1574.

PMID: 38383560 PMC: 10882027. DOI: 10.1038/s41467-024-45954-0.

Targeting ASIC1a Promotes Neural Progenitor Cell Migration and Neurogenesis in Ischemic Stroke.

Ge H, Zhou T, Zhang C, Cun Y, Chen W, Yang Y Research (Wash D C). 2023; 6:0105.

PMID: 37275123 PMC: 10234266. DOI: 10.34133/research.0105.

Critical role and its underlying molecular events of the plasminogen receptor, S100A10 in malignant tumor and non-tumor diseases.

Li C, Ma Y, Fei F, Zheng M, Li Z, Zhao Q J Cancer. 2020; 11(4):826-836.

PMID: 31949486 PMC: 6959022. DOI: 10.7150/jca.36203.

Inhibition of somatosensory mechanotransduction by annexin A6.

Raouf R, Lolignier S, Sexton J, Millet Q, Santana-Varela S, Biller A Sci Signal. 2018; 11(535).

PMID: 29921656 PMC: 6485395. DOI: 10.1126/scisignal.aao2060.

References

Akopian A, Souslova V, England S, Okuse K, Ogata N, Ure J . The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci. 1999; 2(6):541-8. DOI: 10.1038/9195. View

Farley F, Soriano P, Steffen L, Dymecki S . Widespread recombinase expression using FLPeR (flipper) mice. Genesis. 2000; 28(3-4):106-10. View

Renganathan M, Cummins T, Waxman S . Contribution of Na(v)1.8 sodium channels to action potential electrogenesis in DRG neurons. J Neurophysiol. 2001; 86(2):629-40. DOI: 10.1152/jn.2001.86.2.629. View

Kerr B, Souslova V, McMahon S, Wood J . A role for the TTX-resistant sodium channel Nav 1.8 in NGF-induced hyperalgesia, but not neuropathic pain. Neuroreport. 2001; 12(14):3077-80. DOI: 10.1097/00001756-200110080-00019. View

Pawliczak R, Cowan M, Huang X, Nanavaty U, Alsaaty S, Logun C . p11 expression in human bronchial epithelial cells is increased by nitric oxide in a cGMP-dependent pathway involving protein kinase G activation. J Biol Chem. 2001; 276(48):44613-21. DOI: 10.1074/jbc.M104993200. View

Voilley N, De Weille J, Mamet J, Lazdunski M . Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J Neurosci. 2001; 21(20):8026-33. PMC: 6763876. View

Kwon M, Caplan J, Filipenko N, Choi K, Fitzpatrick S, Zhang L . Identification of annexin II heterotetramer as a plasmin reductase. J Biol Chem. 2002; 277(13):10903-11. DOI: 10.1074/jbc.M111219200. View

Gerke V, Moss S . Annexins: from structure to function. Physiol Rev. 2002; 82(2):331-71. DOI: 10.1152/physrev.00030.2001. View

Wemmie J, Chen J, Askwith C, Hruska-Hageman A, Price M, Nolan B . The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron. 2002; 34(3):463-77. DOI: 10.1016/s0896-6273(02)00661-x. View

10.

Okuse K, Malik-Hall M, Baker M, Poon W, Kong H, Chao M . Annexin II light chain regulates sensory neuron-specific sodium channel expression. Nature. 2002; 417(6889):653-6. DOI: 10.1038/nature00781. View

11.

Kretschmer T, Happel L, England J, Nguyen D, Tiel R, Beuerman R . Accumulation of PN1 and PN3 sodium channels in painful human neuroma-evidence from immunocytochemistry. Acta Neurochir (Wien). 2002; 144(8):803-10; discussion 810. DOI: 10.1007/s00701-002-0970-1. View

12.

Girard C, Tinel N, Terrenoire C, Romey G, Lazdunski M, Borsotto M . p11, an annexin II subunit, an auxiliary protein associated with the background K+ channel, TASK-1. EMBO J. 2002; 21(17):4439-48. PMC: 125412. DOI: 10.1093/emboj/cdf469. View

13.

Nicholson R, Small J, Dixon A, Spanswick D, Lee K . Serotonin receptor mRNA expression in rat dorsal root ganglion neurons. Neurosci Lett. 2003; 337(3):119-22. DOI: 10.1016/s0304-3940(02)01256-9. View

14.

Malik-Hall M, Poon W, Baker M, Wood J, Okuse K . Sensory neuron proteins interact with the intracellular domains of sodium channel NaV1.8. Brain Res Mol Brain Res. 2003; 110(2):298-304. DOI: 10.1016/s0169-328x(02)00661-7. View

15.

Huang X, Pawliczak R, Yao X, Cowan M, Gladwin M, Walter M . Interferon-gamma induces p11 gene and protein expression in human epithelial cells through interferon-gamma-activated sequences in the p11 promoter. J Biol Chem. 2003; 278(11):9298-308. DOI: 10.1074/jbc.m212704200. View

16.

van de Graaf S, Hoenderop J, Gkika D, Lamers D, Prenen J, Rescher U . Functional expression of the epithelial Ca(2+) channels (TRPV5 and TRPV6) requires association of the S100A10-annexin 2 complex. EMBO J. 2003; 22(7):1478-87. PMC: 152906. DOI: 10.1093/emboj/cdg162. View

17.

Djouhri L, Fang X, Okuse K, Wood J, Berry C, Lawson S . The TTX-resistant sodium channel Nav1.8 (SNS/PN3): expression and correlation with membrane properties in rat nociceptive primary afferent neurons. J Physiol. 2003; 550(Pt 3):739-52. PMC: 2343087. DOI: 10.1113/jphysiol.2003.042127. View

18.

Roza C, Laird J, Souslova V, Wood J, Cervero F . The tetrodotoxin-resistant Na+ channel Nav1.8 is essential for the expression of spontaneous activity in damaged sensory axons of mice. J Physiol. 2003; 550(Pt 3):921-6. PMC: 2343086. DOI: 10.1113/jphysiol.2003.046110. View

19.

Wemmie J, Askwith C, Lamani E, Cassell M, Freeman Jr J, Welsh M . Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci. 2003; 23(13):5496-502. PMC: 6741257. View

20.

Zobiack N, Rescher U, Ludwig C, Zeuschner D, Gerke V . The annexin 2/S100A10 complex controls the distribution of transferrin receptor-containing recycling endosomes. Mol Biol Cell. 2003; 14(12):4896-908. PMC: 284793. DOI: 10.1091/mbc.e03-06-0387. View