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Research Article

Humanin’s impact on pain markers and neuronal viability in diabetic neuropathy model

ORCID Icon, , , , , , , , , & ORCID Icon show all
Received 05 Sep 2023, Accepted 26 Mar 2024, Published online: 10 Apr 2024

References

  • Basbaum, A.I., et al., 2009. Cellular and molecular mechanisms of pain. Cell, 139 (2), 267–284. doi: 10.1016/j.cell.2009.09.028.
  • Boutari, C., et al., 2022. Humanin and diabetes mellitus: a review of in vitro and in vivo studies. World journal of diabetes, 13 (3), 213–223. doi: 10.4239/wjd.v13.i3.213.
  • Breitinger, U. and Breitinger, H.G., 2023. Excitatory and inhibitory neuronal signaling in inflammatory and diabetic neuropathic pain. Molecular medicine, 29 (1), 53. doi: 10.1186/s10020-023-00647-0.
  • Brenn, D., Richter, F., and Schaible, H.G., 2007. Sensitization of unmyelinated sensory fibers of the joint nerve to mechanical stimuli by interleukin-6 in the rat: an inflammatory mechanism of joint pain. Arthritis and rheumatism, 56 (1), 351–359. doi: 10.1002/art.22282.
  • Bulut, F., et al., 2023. Protective effects of chronic humanin treatment in mice with diabetic encephalopathy: a focus on oxidative stress, inflammation, and apoptosis. Behavioural brain research, 452, 114584. doi: 10.1016/j.bbr.2023.114584.
  • Calcutt, N.A., 2020. Diabetic neuropathy and neuropathic pain: a (con)fusion of pathogenic mechanisms? Pain, 161 (Suppl. 1), S65–S86. doi: 10.1097/j.pain.0000000000001922.
  • Chiba, T., et al., 2005. Development of a femtomolar-acting humanin derivative named colivelin by attaching activity-dependent neurotrophic factor to its N terminus: characterization of colivelin-mediated neuroprotection against Alzheimer’s disease-relevant insults in vitro and in vivo. Journal of neuroscience, 25 (44), 10252–10261. doi: 10.1523/jneurosci.3348-05.2005.
  • Chin, Y.-P., et al., 2013. Pharmacokinetics and tissue distribution of humanin and its analogues in male rodents. Endocrinology, 154 (10), 3739–3744. doi: 10.1210/en.2012-2004.
  • Cunha, F.Q., et al., 1992. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. British journal of pharmacology, 107 (3), 660–664. doi: 10.1111/j.1476-5381.1992.tb14503.x.
  • Deeds, M.C., et al., 2011. Single dose streptozotocin-induced diabetes: considerations for study design in islet transplantation models. Laboratory animals, 45 (3), 131–140. doi: 10.1258/la.2010.010090.
  • Dominguez, E., et al., 2008. JAK/STAT3 pathway is activated in spinal cord microglia after peripheral nerve injury and contributes to neuropathic pain development in rat. Journal of neurochemistry, 107 (1), 50–60. doi: 10.1111/j.1471-4159.2008.05566.x.
  • Dominguez, E., et al., 2010. SOCS3-mediated blockade of JAK/STAT3 signaling pathway reveals its major contribution to spinal cord neuroinflammation and mechanical allodynia after peripheral nerve injury. Journal of neuroscience, 30 (16), 5754–5766. doi: 10.1523/jneurosci.5007-09.2010.
  • Fernyhough, P., 2015. Mitochondrial dysfunction in diabetic neuropathy: a series of unfortunate metabolic events. Current diabetes reports, 15 (11), 89. doi: 10.1007/s11892-015-0671-9.
  • Gilon, C., et al., 2020. Novel humanin analogs confer neuroprotection and myoprotection to neuronal and myoblast cell cultures exposed to ischemia-like and doxorubicin-induced cell death insults. Peptides, 134, 170399. doi: 10.1016/j.peptides.2020.170399.
  • Gottardo, M.F., et al., 2017. Humanin inhibits apoptosis in pituitary tumor cells through several signaling pathways including NF-kappaB activation. Journal of cell communication and signaling, 11 (4), 329–340. doi: 10.1007/s12079-017-0388-4.
  • Green, D. and Reed, J.C., 1998. Mitochondria and apoptosis. Science, 281 (5381), 1309–1312. doi: 10.1126/science.281.5381.1309.
  • Grisold, A., Callaghan, B.C., and Feldman, E.L., 2017. Mediators of diabetic neuropathy: is hyperglycemia the only culprit? Current opinion in endocrinology, diabetes, and obesity, 24 (2), 103–111. doi: 10.1097/MED.0000000000000320.
  • Guo, B., et al., 2003. Humanin peptide suppresses apoptosis by interfering with Bax activation. Nature, 423 (6938), 456–461. doi: 10.1038/nature01627.
  • Hashimoto, Y., et al., 2001a. Detailed characterization of neuroprotection by a rescue factor humanin against various Alzheimer’s disease-relevant insults. Journal of neuroscience, 21 (23), 9235–9245. doi: 10.1523/JNEUROSCI.21-23-09235.2001.
  • Hashimoto, Y., et al., 2001b. A rescue factor abolishing neuronal cell death by a wide spectrum of familial Alzheimer’s disease genes and Aβ. Proceedings of the national academy of sciences of the United States of America, 98 (11), 6336–6341. doi: 10.1073/pnas.101133498.
  • Hashimoto, Y., et al., 2005. Involvement of tyrosine kinases and STAT3 in humanin-mediated neuroprotection. Life sciences, 77 (24), 3092–3104. doi: 10.1016/j.lfs.2005.03.031.
  • Hashimoto, Y., et al., 2009a. Humanin inhibits neuronal cell death by interacting with a cytokine receptor complex or complexes involving CNTF receptor alpha/WSX-1/gp130. Molecular biology of the cell, 20 (12), 2864–2873. doi: 10.1091/mbc.e09-02-0168.
  • Hashimoto, Y., Kurita, M., and Matsuoka, M., 2009b. Identification of soluble WSX-1 not as a dominant-negative but as an alternative functional subunit of a receptor for an anti-Alzheimer’s disease rescue factor Humanin. Biochemical and biophysical research communications, 389 (1), 95–99. doi: 10.1016/j.bbrc.2009.08.095.
  • Hazafa, A., et al., 2021. Humanin: a mitochondrial-derived peptide in the treatment of apoptosis-related diseases. Life sciences, 264, 118679. doi: 10.1016/j.lfs.2020.118679.
  • Hekim, M.G., et al., 2023. Asprosin, a novel glucogenic adipokine: a potential therapeutic implication in diabetes mellitus. Archives of physiology and biochemistry, 129 (5), 1038–1044. doi: 10.1080/13813455.2021.1894178.
  • Hoang, P.T., et al., 2010. The neurosurvival factor humanin inhibits beta-cell apoptosis via signal transducer and activator of transcription 3 activation and delays and ameliorates diabetes in nonobese diabetic mice. Metabolism: clinical and experimental, 59 (3), 343–349. doi: 10.1016/j.metabol.2009.08.001.
  • Holtzman, D.M. and Deshmukh, M., 1997. Caspases: a treatment target for neurodegenerative disease? Nature medicine, 3 (9), 954–955. doi: 10.1038/nm0997-954.
  • Ikonen, M., et al., 2003. Interaction between the Alzheimer’s survival peptide humanin and insulin-like growth factor-binding protein 3 regulates cell survival and apoptosis. Proceedings of the national academy of sciences of the United States of America, 100 (22), 13042–13047. doi: 10.1073/pnas.2135111100.
  • Kariya, S., et al., 2002. Humanin inhibits cell death of serum-deprived PC12h cells. Neuroreport, 13 (6), 903–907. doi: 10.1097/00001756-200205070-00034.
  • Khuankaew, C., et al., 2021. Possible roles of mitochondrial dysfunction in neuropathy. International journal of neuroscience, 131 (10), 1019–1041. doi: 10.1080/00207454.2020.1765777.
  • Kin, T., et al., 2006. Humanin expression in skeletal muscles of patients with chronic progressive external ophthalmoplegia. Journal of human genetics, 51 (6), 555–558. doi: 10.1007/s10038-006-0397-2.
  • Kuliawat, R., et al., 2013. Potent humanin analog increases glucose-stimulated insulin secretion through enhanced metabolism in the beta cell. FASEB journal, 27 (12), 4890–4898. doi: 10.1096/fj.13-231092.
  • Liu, Y., et al., 2019. CGRP reduces apoptosis of DRG cells induced by high-glucose oxidative stress injury through PI3K/AKT induction of heme oxygenase-1 and Nrf-2 expression. Oxidative medicine and cellular longevity, 2019, 2053149. doi: 10.1155/2019/2053149.
  • Lue, Y., et al., 2010. Opposing roles of insulin-like growth factor binding protein 3 and humanin in the regulation of testicular germ cell apoptosis. Endocrinology, 151 (1), 350–357. doi: 10.1210/en.2009-0577.
  • Ma, Z.W. and Liu, D.X., 2018. Humanin decreases mitochondrial membrane permeability by inhibiting the membrane association and oligomerization of Bax and Bid proteins. Acta pharmacologica sinica, 39 (6), 1012–1021. doi: 10.1038/aps.2017.169.
  • Matsuoka, M. and Hashimoto, Y., 2010. Humanin and the receptors for humanin. Molecular neurobiology, 41 (1), 22–28. doi: 10.1007/s12035-009-8090-z.
  • Matsuoka, M., 2009. Humanin; a defender against Alzheimer’s disease? Recent patents on CNS drug discovery, 4 (1), 37–42. doi: 10.2174/157488909787002609.
  • Melemedjian, O.K., et al., 2010. IL-6- and NGF-induced rapid control of protein synthesis and nociceptive plasticity via convergent signaling to the eIF4F complex. Journal of neuroscience, 30 (45), 15113–15123. doi: 10.1523/jneurosci.3947-10.2010.
  • Melemedjian, O.K., et al., 2014. Local translation and retrograde axonal transport of CREB regulates IL-6-induced nociceptive plasticity. Molecular pain, 10, 45. doi: 10.1186/1744-8069-10-45.
  • Mohiuddin, M.S., et al., 2019. Glucagon-like peptide-1 receptor agonist protects dorsal root ganglion neurons against oxidative insult. Journal of diabetes research, 2019, 9426014. doi: 10.1155/2019/9426014.
  • Muzumdar, R.H., et al., 2009. Humanin: a novel central regulator of peripheral insulin action. PLOS one, 4 (7), e6334. doi: 10.1371/journal.pone.0006334.
  • Muzumdar, R.H., et al., 2010. Acute humanin therapy attenuates myocardial ischemia and reperfusion injury in mice. Arteriosclerosis, thrombosis, and vascular biology, 30 (10), 1940–1948. doi: 10.1161/ATVBAHA.110.205997.
  • Nishimoto, I., Matsuoka, M., and Niikura, T., 2004. Unravelling the role of humanin. Trends in molecular medicine, 10 (3), 102–105. doi: 10.1016/j.molmed.2004.01.001.
  • Obreja, O., et al., 2002. Interleukin-6 in combination with its soluble IL-6 receptor sensitises rat skin nociceptors to heat, in vivo. Pain, 96 (1–2), 57–62. doi: 10.1016/s0304-3959(01)00420-1.
  • Ozcan, M., et al., 2010. Effects of levobupivacaine and bupivacaine on intracellular calcium signaling in cultured rat dorsal root ganglion neurons. Journal of receptor and signal transduction research, 30 (2), 115–120. doi: 10.3109/10799891003630614.
  • Ozcan, M., et al., 2019. Agomelatine pretreatment prevents development of hyperglycemia and hypoinsulinemia in streptozotocin‐induced diabetes in mice. Fundamental & clinical pharmacology, 33 (2), 170–180. doi: 10.1111/fcp.12413.
  • Ozcan, S., et al., 2020. Agomelatine potentiates anti-nociceptive effects of morphine in a mice model for diabetic neuropathy: involvement of NMDA receptor subtype NR1 within the raphe nucleus and periaqueductal grey. Neurological research, 42 (7), 554–563. doi: 10.1080/01616412.2020.1757895.
  • Ozcan, S., et al., 2022. Asprosin, a novel therapeutic candidate for painful neuropathy: an experimental study in mice. Naunyn-Schmiedeberg’s archives of pharmacology, 395 (3), 325–335. doi: 10.1007/s00210-021-02197-w.
  • Park, T.-Y., et al., 2013. Amelioration of neurodegenerative diseases by cell death-induced cytoplasmic delivery of humanin. Journal of controlled release, 166 (3), 307–315. doi: 10.1016/j.jconrel.2012.12.022.
  • Pope, J.E., Deer, T.R., and Kramer, J., 2013. A systematic review: current and future directions of dorsal root ganglion therapeutics to treat chronic pain. Pain medicine, 14 (10), 1477–1496. doi: 10.1111/pme.12171.
  • Ramanjaneya, M., et al., 2019. Mitochondrial-derived peptides are down regulated in diabetes subjects. Frontiers in endocrinology, 10, 331. doi: 10.3389/fendo.2019.00331.
  • Ribeiro, H., et al., 2022. Apoptosis and (in) pain—potential clinical implications. Biomedicines, 10 (6), 1255. doi: 10.3390/biomedicines10061255.
  • Sponne, I., et al., 2004. Humanin rescues cortical neurons from prion-peptide-induced apoptosis. Molecular and cellular neurosciences, 25 (1), 95–102. doi: 10.1016/j.mcn.2003.09.017.
  • Vazquez, E., et al., 2012. Spinal interleukin-6 is an amplifier of arthritic pain in the rat. Arthritis and rheumatism, 64 (7), 2233–2242. doi: 10.1002/art.34384.
  • Vincent, A.M., et al., 2011. Diabetic neuropathy: cellular mechanisms as therapeutic targets. Nature reviews. Neurology, 7 (10), 573–583. doi: 10.1038/nrneurol.2011.137.
  • Vyklický, L. and Knotková-Urbancovä, H., 1996. Can sensory neurones in culture serve as a model of nociception? Physiological research, 45, 1–9.
  • Wang, D., et al., 2005. Humanin delays apoptosis in K562 cells by downregulation of P38 MAP kinase. Apoptosis, 10 (5), 963–971. doi: 10.1007/s10495-005-1191-x.
  • Xu, X., et al., 2006. Humanin is a novel neuroprotective agent against stroke. Stroke, 37 (10), 2613–2619. doi: 10.1161/01.STR.0000242772.94277.1f.
  • Yagihashi, S., Mizukami, H., and Sugimoto, K., 2011. Mechanism of diabetic neuropathy: where are we now and where to go? Journal of diabetes investigation, 2 (1), 18–32. doi: 10.1111/j.2040-1124.2010.00070.x.
  • Yen, K., et al., 2018. Humanin prevents age-related cognitive decline in mice and is associated with improved cognitive age in humans. Scientific reports, 8 (1), 14212. doi: 10.1038/s41598-018-32616-7.
  • Zapała, B., et al., 2010. Humanins, the neuroprotective and cytoprotective peptides with antiapoptotic and anti-inflammatory properties. Pharmacological reports, 62 (5), 767–777. doi: 10.1016/s1734-1140(10)70337-6.
  • Zhai, D., et al., 2005. Humanin binds and nullifies Bid activity by blocking its activation of Bax and Bak. Journal of biological chemistry, 280 (16), 15815–15824. doi: 10.1074/jbc.M411902200.
  • Zhao, S.T., et al., 2012. Humanin protects cortical neurons from ischemia and reperfusion injury by the increased activity of superoxide dismutase. Neurochemical research, 37 (1), 153–160. doi: 10.1007/s11064-011-0593-0.

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