Implication of thermal signaling in neuronal differentiation revealed by manipulation and measurement of intracellular temperature.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
09 May 2024
09 May 2024
Historique:
received:
08
06
2023
accepted:
28
03
2024
medline:
10
5
2024
pubmed:
10
5
2024
entrez:
9
5
2024
Statut:
epublish
Résumé
Neuronal differentiation-the development of neurons from neural stem cells-involves neurite outgrowth and is a key process during the development and regeneration of neural functions. In addition to various chemical signaling mechanisms, it has been suggested that thermal stimuli induce neuronal differentiation. However, the function of physiological subcellular thermogenesis during neuronal differentiation remains unknown. Here we create methods to manipulate and observe local intracellular temperature, and investigate the effects of noninvasive temperature changes on neuronal differentiation using neuron-like PC12 cells. Using quantitative heating with an infrared laser, we find an increase in local temperature (especially in the nucleus) facilitates neurite outgrowth. Intracellular thermometry reveals that neuronal differentiation is accompanied by intracellular thermogenesis associated with transcription and translation. Suppression of intracellular temperature increase during neuronal differentiation inhibits neurite outgrowth. Furthermore, spontaneous intracellular temperature elevation is involved in neurite outgrowth of primary mouse cortical neurons. These results offer a model for understanding neuronal differentiation induced by intracellular thermal signaling.
Identifiants
pubmed: 38724563
doi: 10.1038/s41467-024-47542-8
pii: 10.1038/s41467-024-47542-8
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3473Subventions
Organisme : MEXT | Japan Society for the Promotion of Science (JSPS)
ID : 20H05785
Informations de copyright
© 2024. The Author(s).
Références
Temple, S. The development of neural stem cells. Nature 414, 112–117 (2001).
pubmed: 11689956
doi: 10.1038/35102174
Arimura, N. & Kaibuchi, K. Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8, 194–205 (2007).
pubmed: 17311006
doi: 10.1038/nrn2056
Yogev, S. & Shen, K. Establishing neuronal polarity with environmental and intrinsic mechanisms. Neuron 96, 638–650 (2017).
pubmed: 29096077
doi: 10.1016/j.neuron.2017.10.021
Bond, A. M., Ming, G. L. & Song, H. Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell 17, 385–395 (2015).
pubmed: 26431181
pmcid: 4683085
doi: 10.1016/j.stem.2015.09.003
Bäckman, C. et al. Systemic administration of a nerve growth factor conjugate reverses age- related cognitive dysfunction and prevents cholinergic neuron atrophy. J. Neurosci. 16, 5437–5442 (1996).
pubmed: 8757256
pmcid: 6578877
doi: 10.1523/JNEUROSCI.16-17-05437.1996
Burns, T. C. & Quinones-Hinojosa, A. Regenerative medicine for neurological diseases - will regenerative neurosurgery deliver? BMJ 373, n955 (2021).
pubmed: 34162530
doi: 10.1136/bmj.n955
Skaper, S. D. The neurotrophin family of neurotrophic factors: an overview. Methods Mol. Biol. 846, 1–12 (2012).
pubmed: 22367796
doi: 10.1007/978-1-61779-536-7_1
Park, H. & Poo, M. Neurotrophin regulation of neural circuit development and function. Nat. Rev. Neurosci. 14, 7–23 (2013).
pubmed: 23254191
doi: 10.1038/nrn3379
Reichardt, L. F. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. B Biol. Sci. 361, 1545–1564 (2006).
doi: 10.1098/rstb.2006.1894
Clark, S. E., Moss, D. J. & Bray, D. Actin polymerization and synthesis in cultured neurones. Exp. Cell Res. 147, 303–314 (1983).
pubmed: 6225655
doi: 10.1016/0014-4827(83)90213-6
Zhou, F. Q., Zhou, J., Dedhar, S., Wu, Y. H. & Snider, W. D. NGF-induced axon growth is mediated by localized inactivation of GSK-3β and functions of the microtubule plus end binding protein APC. Neuron 42, 897–912 (2004).
pubmed: 15207235
doi: 10.1016/j.neuron.2004.05.011
Yuan, X. B. et al. Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat. Cell Biol. 5, 38–45 (2003).
pubmed: 12510192
doi: 10.1038/ncb895
Lowery, L. A. & Vactor Van, D. The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 10, 332–343 (2009).
pubmed: 19373241
pmcid: 2714171
doi: 10.1038/nrm2679
Shibasaki, K., Murayama, N., Ono, K., Ishizaki, Y. & Tominaga, M. TRPV2 enhances axon outgrowth through its activation by membrane stretch in developing sensory and motor neurons. J. Neurosci. 30, 4601–4612 (2010).
pubmed: 20357111
pmcid: 6632311
doi: 10.1523/JNEUROSCI.5830-09.2010
de Vincentiis, S. et al. Extremely low forces induce extreme axon growth. J. Neurosci. 40, 4997–5007 (2020).
pubmed: 32444384
pmcid: 7314409
doi: 10.1523/JNEUROSCI.3075-19.2020
Cheng, H., Huang, Y., Yue, H. & Fan, Y. Electrical stimulation promotes stem cell neural differentiation in tissue engineering. Stem Cells Int. 2021, 6697574 (2021).
pubmed: 33968150
pmcid: 8081629
doi: 10.1155/2021/6697574
Xu, K. et al. Effect of electrical and electromechanical stimulation on PC12 cell proliferation and axon outgrowth. Front. Bioeng. Biotechnol. 9, 757906 (2021).
pubmed: 34746110
pmcid: 8566739
doi: 10.3389/fbioe.2021.757906
Black, B. J., Gu, L. & Mohanty, S. K. Highly effective photonic cue for repulsive axonal guidance. PLoS ONE 9, e86292 (2014).
pubmed: 24717339
pmcid: 3981697
doi: 10.1371/journal.pone.0086292
Black, B., Mondal, A., Kim, Y. & Mohanty, S. K. Neuronal beacon. Opt. Lett. 38, 2174 (2013).
pubmed: 23811868
doi: 10.1364/OL.38.002174
Kao, Y.-C., Liao, Y.-C., Cheng, P.-L. & Lee, C.-H. Neurite regrowth stimulation by a red-light spot focused on the neuronal cell soma following blue light-induced retraction. Sci. Rep. 9, 18210 (2019).
pubmed: 31796850
pmcid: 6890775
doi: 10.1038/s41598-019-54687-w
Wang, J.-L., Lin, Y.-C., Young, T.-H. & Chen, M.-H. Far-infrared ray radiation promotes neurite outgrowth of neuron-like PC12 cells through AKT1 signaling. J. Formos. Med. Assoc. 118, 600–610 (2019).
pubmed: 30173931
doi: 10.1016/j.jfma.2018.08.015
Hoshi, Y., Shibasaki, K., Gailly, P., Ikegaya, Y. & Koyama, R. Thermosensitive receptors in neural stem cells link stress-induced hyperthermia to impaired neurogenesis via microglial engulfment. Sci. Adv. 7, eabj8080 (2021).
pubmed: 34826234
pmcid: 8626080
doi: 10.1126/sciadv.abj8080
Blasa, S. et al. Prussian blue nanoparticle-mediated scalable thermal stimulation for in vitro neuronal differentiation. Nanomaterials 12, 2304 (2022).
Antonova, O. Y., Kochetkova, O. Y. & Kanev, I. L. Light-to-heat converting ECM-mimetic nanofiber scaffolds for neuronal differentiation and neurite outgrowth guidance. Nanomaterials 12, 2166 (2022).
pubmed: 35808000
pmcid: 9268234
doi: 10.3390/nano12132166
Kudo, T. et al. Induction of neurite outgrowth in PC12 cells treated with temperature-controlled repeated thermal stimulation. PLoS ONE 10, e0124024 (2015).
pubmed: 25879210
pmcid: 4399938
doi: 10.1371/journal.pone.0124024
Oyama, K. et al. Triggering of high-speed neurite outgrowth using an optical microheater. Sci. Rep. 5, 16611 (2015).
pubmed: 26568288
pmcid: 4645119
doi: 10.1038/srep16611
Black, B. et al. Spatial temperature gradients guide axonal outgrowth. Sci. Rep. 6, 29876 (2016).
pubmed: 27460512
pmcid: 4962095
doi: 10.1038/srep29876
Read, D. E., Reed Herbert, K. & Gorman, A. M. Heat shock enhances NGF-induced neurite elongation which is not mediated by Hsp25 in PC12 cells. Brain Res. 1221, 14–23 (2008).
pubmed: 18561899
doi: 10.1016/j.brainres.2008.05.028
Hossain, M. E. et al. Direct exposure to mild heat promotes proliferation and neuronal differentiation of neural stem/progenitor cells in vitro. PLoS ONE 12, e0190356 (2017).
pubmed: 29287093
pmcid: 5747471
doi: 10.1371/journal.pone.0190356
Refinetti, R. & Menaker, M. The circadian rhythm of body temperature. Physiol. Behav. 51, 613–637 (1992).
pubmed: 1523238
doi: 10.1016/0031-9384(92)90188-8
Cagnacci, A., Soldani, R., Laughlin, G. A. & Yen, S. S. C. Modification of circadian body temperature rhythm during the luteal menstrual phase: Role of melatonin. J. Appl. Physiol. 80, 25–29 (1996).
pubmed: 8847311
doi: 10.1152/jappl.1996.80.1.25
Rzechorzek, N. M. et al. A daily temperature rhythm in the human brain predicts survival after brain injury. Brain 145, 2031–2048 (2022).
pubmed: 35691613
pmcid: 9336587
doi: 10.1093/brain/awab466
Kiyatkin, E. A. Brain temperature and its role in physiology and pathophysiology: Lessons from 20 years of thermorecording. Temperature 6, 271–333 (2019).
doi: 10.1080/23328940.2019.1691896
Okabe, K. et al. Intracellular temperature mapping with a fluorescent polymeric thermometer and fluorescence lifetime imaging microscopy. Nat. Commun. 3, 705 (2012).
pubmed: 22426226
doi: 10.1038/ncomms1714
Okabe, K., Sakaguchi, R., Shi, B. & Kiyonaka, S. Intracellular thermometry with fluorescent sensors for thermal biology. Pflügers. Arch. Eur. J. Physiol. 470, 717–731 (2018).
doi: 10.1007/s00424-018-2113-4
Zhou, J., del Rosal, B., Jaque, D., Uchiyama, S. & Jin, D. Advances and challenges for fluorescence nanothermometry. Nat. Methods 17, 967–980 (2020).
pubmed: 32989319
doi: 10.1038/s41592-020-0957-y
Hayashi, T., Fukuda, N., Uchiyama, S. & Inada, N. A cell-permeable fluorescent polymeric thermometer for intracellular temperature mapping in mammalian cell lines. PLoS ONE 10, e0117677 (2015).
pubmed: 25692871
pmcid: 4333297
doi: 10.1371/journal.pone.0117677
Hoshi, Y. et al. Ischemic brain injury leads to brain edema via hyperthermia-induced TRPV4 activation. J. Neurosci. 38, 5700–5709 (2018).
pubmed: 29793978
pmcid: 6595977
doi: 10.1523/JNEUROSCI.2888-17.2018
Petrini, G. et al. Nanodiamond-quantum sensors reveal temperature variation associated to hippocampal neurons firing. Adv. Sci. 9, e2202014 (2022).
Tanimoto, R. et al. Detection of temperature difference in neuronal cells. Sci. Rep. 6, 22071 (2016).
pubmed: 26925874
pmcid: 4772094
doi: 10.1038/srep22071
Okabe, K. & Uchiyama, S. Intracellular thermometry uncovers spontaneous thermogenesis and associated thermal signaling. Commun. Biol. 4, 1377 (2021).
pubmed: 34887517
pmcid: 8660847
doi: 10.1038/s42003-021-02908-2
Choi, J. et al. Probing and manipulating embryogenesis via nanoscale thermometry and temperature control. Proc. Natl. Acad. Sci. USA 117, 14636–14641 (2020).
pubmed: 32541064
pmcid: 7334529
doi: 10.1073/pnas.1922730117
Ermakova, Y. G. et al. Thermogenetic neurostimulation with single-cell resolution. Nat. Commun. 8, 15362 (2017).
pubmed: 28530239
pmcid: 5493594
doi: 10.1038/ncomms15362
Marino, A. et al. Gold nanoshell-mediated remote myotube activation. ACS Nano 11, 2494–2505 (2017).
pubmed: 28107625
doi: 10.1021/acsnano.6b08202
Kamei, Y. et al. Infrared laser-mediated gene induction in targeted single cells in vivo. Nat. Methods 6, 79–81 (2009).
pubmed: 19079252
doi: 10.1038/nmeth.1278
Sotoma, S. et al. In situ measurements of intracellular thermal conductivity using heater-thermometer hybrid diamond nanosensors. Sci. Adv. 7, eabd7888 (2021).
pubmed: 33523906
pmcid: 7810374
doi: 10.1126/sciadv.abd7888
Fujiwara, M. et al. Real-time nanodiamond thermometry probing in vivo thermogenic responses. Sci. Adv. 6, eaba9636 (2020).
pubmed: 32917703
pmcid: 7486095
doi: 10.1126/sciadv.aba9636
Ding, Y., Ye, X. & Zhang, G. Microcalorimetric investigation on aggregation and dissolution of poly(N-isopropylacrylamide) chains in water. Macromolecules 38, 904–908 (2005).
doi: 10.1021/ma048460q
Hartgill, T. W., Bergersen, T. K. & Pirhonen, J. Core body temperature and the thermoneutral zone: A longitudinal study of normal human pregnancy. Acta Physiol. 201, 467–474 (2011).
doi: 10.1111/j.1748-1716.2010.02228.x
Sekiguchi, T., Sotoma, S. & Harada, Y. Fluorescent nanodiamonds as a robust temperature sensor inside a single cell. Biophys. Physicobiol. 15, 229–234 (2018).
pubmed: 30450272
pmcid: 6234897
doi: 10.2142/biophysico.15.0_229