ALPK1 Expressed in IB4-Positive Neurons of Mice Trigeminal Ganglions Promotes MIA-Induced TMJ pain

doi:10.1007/s12035-023-03462-0

. 2023 Nov;60(11):6264-6274.

doi: 10.1007/s12035-023-03462-0. Epub 2023 Jul 13.

ALPK1 Expressed in IB4-Positive Neurons of Mice Trigeminal Ganglions Promotes MIA-Induced TMJ pain

Taomin Zhu^#^{1

2}, Huimin Li^#^{1

2}, Yuxiang Chen^#³, Xueke Jia^{1

2}, Xiaohan Ma^{1

2}, Xin Liu^{1

2}, Yaping Feng^{1

2}, Jin Ke^{4

5}

Affiliations

¹ The State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) & Key Laboratory of Oral Biomedicine Ministry of Education, School & Hospital of Stomatology, Wuhan University, 237 Luoyu Road, Wuhan, 430079, Hubei Province, China.
² Department of Oral and Maxillofacial Trauma and Temporomandibular Joint Surgery, Hubei-MOST KLOS & KLOBM, School & Hospital of Stomatology, Wuhan University, Wuhan, 430079, China.
³ GuangDong Women and Children Hospital, Guangdong, 511400, China.
⁴ The State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) & Key Laboratory of Oral Biomedicine Ministry of Education, School & Hospital of Stomatology, Wuhan University, 237 Luoyu Road, Wuhan, 430079, Hubei Province, China. [email protected].
⁵ Department of Oral and Maxillofacial Trauma and Temporomandibular Joint Surgery, Hubei-MOST KLOS & KLOBM, School & Hospital of Stomatology, Wuhan University, Wuhan, 430079, China. [email protected].

^# Contributed equally.

PMID: 37442857
DOI: 10.1007/s12035-023-03462-0

ALPK1 Expressed in IB4-Positive Neurons of Mice Trigeminal Ganglions Promotes MIA-Induced TMJ pain

Taomin Zhu et al. Mol Neurobiol. 2023 Nov.

. 2023 Nov;60(11):6264-6274.

doi: 10.1007/s12035-023-03462-0. Epub 2023 Jul 13.

Authors

Taomin Zhu^#^{1

2}, Huimin Li^#^{1

2}, Yuxiang Chen^#³, Xueke Jia^{1

2}, Xiaohan Ma^{1

2}, Xin Liu^{1

2}, Yaping Feng^{1

2}, Jin Ke^{4

5}

Affiliations

¹ The State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) & Key Laboratory of Oral Biomedicine Ministry of Education, School & Hospital of Stomatology, Wuhan University, 237 Luoyu Road, Wuhan, 430079, Hubei Province, China.
² Department of Oral and Maxillofacial Trauma and Temporomandibular Joint Surgery, Hubei-MOST KLOS & KLOBM, School & Hospital of Stomatology, Wuhan University, Wuhan, 430079, China.
³ GuangDong Women and Children Hospital, Guangdong, 511400, China.
⁴ The State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) & Key Laboratory of Oral Biomedicine Ministry of Education, School & Hospital of Stomatology, Wuhan University, 237 Luoyu Road, Wuhan, 430079, Hubei Province, China. [email protected].
⁵ Department of Oral and Maxillofacial Trauma and Temporomandibular Joint Surgery, Hubei-MOST KLOS & KLOBM, School & Hospital of Stomatology, Wuhan University, Wuhan, 430079, China. [email protected].

^# Contributed equally.

PMID: 37442857
DOI: 10.1007/s12035-023-03462-0

Abstract

Pain is one of the main reasons for patients with temporomandibular joint (TMJ) disorders seeking medical care. However, there is no effective treatment yet as its mechanism remains unclear. Herein, we found that the injection of monoiodoacetate (MIA) into mice TMJs can induce typical joint pain as early as 3 days, accompanied by an increased percentage of calcitonin gene-related peptide positive (CGRP⁺) neurons and isolectin B4 positive (IB4⁺) in the trigeminal ganglions (TGs). Our previous study has discovered that alpha-kinase 1 (ALPK1) may be involved in joint pain. Here, we detected the expression of ALPK1 in neurons of TGs in wild-type (WT) mice, and it was upregulated after intra-TMJ injection of MIA. Meanwhile, the increased percentage of neurons in TGs expressing ALPK1 and CGRP or ALPK1 and IB4 was also demonstrated by the immunofluorescent double staining. Furthermore, after the MIA injection, ALPK1^-/- mice exhibited attenuated pain behavior, as well as a remarkably decreased percentage of IB4⁺ neurons and an unchanged percentage of CGRP⁺ neurons, as compared with WT mice. In vitro assay showed that the value of calcium intensity was weakened in Dil⁺ neurons from ALPK1^-/- mice of TMJ pain induced by the MIA injection, in relation to those from WT mice, while it was significantly enhanced with the incubation of recombinant human ALPK1 (rhA). Taken together, these results suggest that ALPK1 promotes mice TMJ pain induced by MIA through upregulation of the sensitization of IB4⁺ neurons in TGs. This study will provide a new potential therapeutic target for the treatment of TMJ pain.

Keywords: Alpha-kinase 1 (ALPK1); Pain; Peripheral nociceptive system; Temporomandibular joint (TMJ); Trigeminal ganglion.

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References

1. Auerbach SM, Laskin DM, Frantsve LM, Orr T (2001) Depression, pain, exposure to stressful life events, and long-term outcomes in temporomandibular disorder patients. J Oral Maxillofac Surg 59 (6):628–633; discussion 634. https://doi.org/10.1053/joms.2001.23371
1. Schiffman E, Ohrbach R, Truelove E, Look J, Anderson G, Goulet JP, List T, Svensson P et al (2014) Diagnostic criteria for temporomandibular disorders (DC/TMD) for clinical and research applications: recommendations of the International RDC/TMD Consortium Network* and Orofacial Pain Special Interest Group†. J Oral Facial Pain Headache 28(1):6–27. https://doi.org/10.11607/jop.1151 - DOI - PubMed - PMC
1. Slade GD, Ohrbach R, Greenspan JD, Fillingim RB, Bair E, Sanders AE, Dubner R, Diatchenko L, et al (2016) Painful temporomandibular disorder: decade of discovery from OPPERA studies. J Dent Res 95(10):1084–1092. https://doi.org/10.1177/0022034516653743 - DOI - PubMed - PMC
1. Wang X, Zhang J, Gan Y, Zhou Y (2015) Current understanding of pathogenesis and treatment of TMJ osteoarthritis. J Dent Res 94(5):666–673. https://doi.org/10.1177/0022034515574770 - DOI - PubMed
1. O’Neil C, Hanlon J, Marcum Z (2012) Adverse effects of analgesics commonly used by older adults with osteoarthritis: focus on non-opioid and opioid analgesics. Am J Geriatr Pharmacother 10(6):331–342. https://doi.org/10.1016/j.amjopharm.2012.09.004 - DOI - PubMed - PMC

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[1] Auerbach SM, Laskin DM, Frantsve LM, Orr T (2001) Depression, pain, exposure to stressful life events, and long-term outcomes in temporomandibular disorder patients. J Oral Maxillofac Surg 59 (6):628–633; discussion 634. https://doi.org/10.1053/joms.2001.23371

[2] Auerbach SM, Laskin DM, Frantsve LM, Orr T (2001) Depression, pain, exposure to stressful life events, and long-term outcomes in temporomandibular disorder patients. J Oral Maxillofac Surg 59 (6):628–633; discussion 634. https://doi.org/10.1053/joms.2001.23371

[3] Schiffman E, Ohrbach R, Truelove E, Look J, Anderson G, Goulet JP, List T, Svensson P et al (2014) Diagnostic criteria for temporomandibular disorders (DC/TMD) for clinical and research applications: recommendations of the International RDC/TMD Consortium Network* and Orofacial Pain Special Interest Group†. J Oral Facial Pain Headache 28(1):6–27. https://doi.org/10.11607/jop.1151 - DOI - PubMed - PMC

[4] Schiffman E, Ohrbach R, Truelove E, Look J, Anderson G, Goulet JP, List T, Svensson P et al (2014) Diagnostic criteria for temporomandibular disorders (DC/TMD) for clinical and research applications: recommendations of the International RDC/TMD Consortium Network* and Orofacial Pain Special Interest Group†. J Oral Facial Pain Headache 28(1):6–27. https://doi.org/10.11607/jop.1151 - DOI - PubMed - PMC

[5] Slade GD, Ohrbach R, Greenspan JD, Fillingim RB, Bair E, Sanders AE, Dubner R, Diatchenko L, et al (2016) Painful temporomandibular disorder: decade of discovery from OPPERA studies. J Dent Res 95(10):1084–1092. https://doi.org/10.1177/0022034516653743 - DOI - PubMed - PMC

[6] Slade GD, Ohrbach R, Greenspan JD, Fillingim RB, Bair E, Sanders AE, Dubner R, Diatchenko L, et al (2016) Painful temporomandibular disorder: decade of discovery from OPPERA studies. J Dent Res 95(10):1084–1092. https://doi.org/10.1177/0022034516653743 - DOI - PubMed - PMC

[7] Wang X, Zhang J, Gan Y, Zhou Y (2015) Current understanding of pathogenesis and treatment of TMJ osteoarthritis. J Dent Res 94(5):666–673. https://doi.org/10.1177/0022034515574770 - DOI - PubMed

[8] Wang X, Zhang J, Gan Y, Zhou Y (2015) Current understanding of pathogenesis and treatment of TMJ osteoarthritis. J Dent Res 94(5):666–673. https://doi.org/10.1177/0022034515574770 - DOI - PubMed

[9] O’Neil C, Hanlon J, Marcum Z (2012) Adverse effects of analgesics commonly used by older adults with osteoarthritis: focus on non-opioid and opioid analgesics. Am J Geriatr Pharmacother 10(6):331–342. https://doi.org/10.1016/j.amjopharm.2012.09.004 - DOI - PubMed - PMC

[10] O’Neil C, Hanlon J, Marcum Z (2012) Adverse effects of analgesics commonly used by older adults with osteoarthritis: focus on non-opioid and opioid analgesics. Am J Geriatr Pharmacother 10(6):331–342. https://doi.org/10.1016/j.amjopharm.2012.09.004 - DOI - PubMed - PMC

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ALPK1 Expressed in IB4-Positive Neurons of Mice Trigeminal Ganglions Promotes MIA-Induced TMJ pain

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ALPK1 Expressed in IB4-Positive Neurons of Mice Trigeminal Ganglions Promotes MIA-Induced TMJ pain

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