Epidermal Keratinocyte Sensing and Processing of Environmental Information Together with the Brain’s Simulation and Prediction Abilities Helped to Enable <i>Homo sapiens’</i> Evolutionary Success — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Epidermal Keratinocyte Sensing and Processing of Environmental Information Together with the Brain’s Simulation and Prediction Abilities Helped to Enable <i>Homo sapiens’</i> Evolutionary Success
Japan Science and Technology Agency, CREST, Kawaguchi, Japan
,
Japan and Shiseido Global Innovation Center, Yokohama, Japan
1 Japan Science and Technology Agency, CREST, Kawaguchi, Japan
2 Japan and Shiseido Global Innovation Center, Yokohama, Japan
Among terrestrial mammals, Homo sapiens has evolved a very specific anatomical feature—very little body hair—thus, the skin surface is exposed directly to the environment. We and others have demonstrated that skin epithelial cells, called keratinocytes, express not only functional sensory systems for a variety of environmental responses, but also a series of neurotransmitter receptors that play key roles in information processing in the brain. Furthermore, the brain cortex is particularly large in Homo sapiens , which has a higher ratio of brain to whole-body weight than any other mammalian species. Here we propose that the evolutionary success and global spread of Homo sapiens are due at least in part to the existence and interaction of these two systems; i.e. the epidermis and brain cortex. First, we discuss the role of the epidermis as a sophisticated organ with multiple sensory inputs and information-processing capabilities, and then we consider the putative requirement for a large brain to carry out simulations and predictions based on input from multiple epidermal systems. We also present some other examples where a functionally sophisticated epidermis is associated with a large brain size. Finally, we discuss possible reasons why Homo sapiens has emerged as the sole surviving human subspecies.
KeywordsSkinBrain CortexBody HairNeurotransmitter
Bhagwandin, A., Haagensen, M., & Manger, P.R. (2017). The Brain of the Black (Diceros bicornis) and White (Ceratotherium simum) African Rhinoceroses: Morphology and Volumetrics from Magnetic Resonance Imaging. Frontiers in Neuroanatomy, 11, 74. https://doi.org/10.3389/fnana.2017.00074
Blanton, C. M., & Ewel, J. J. (1985). Leaf-Cutting ant Herbivory in Successional and Agricultural Tropical Ecosystems. Ecology, 66, 861-869. https://doi.org/10.2307/1940548
Boutin, A. T., Weidemann, A. Z., Fu, L., Mesropian, K., Gradin, C., Jamora, M., Wiesener, K. U., Eckardt, C. J. et al. (2008). Epidermal Sensing of Oxygen Is Essential for Systemic Hypoxic Response. Cell, 133, 223-234. https://doi.org/10.1016/j.cell.2008.02.038
Busse, D., Kudella, P., Grüning, N. M., Gisselmann, G., Ständer, S., Luger, T. et al. (2014). A Synthetic Sandalwood Odorant Induces Wound-Healing Processes in Human Keratinocytes via the Olfactory Receptor OR2AT4. Journal of Investigative Dermatology, 134, 2823-2832. https://doi.org/10.1038/jid.2014.273
Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., & Julius, D. (1997). The Capsaicin Receptor: A Heat-Activated Ion Channel in the Pain Pathway. Nature, 389, 816-824. https://doi.org/10.1038/39807
Cha, Y., Murray, C. J., & Klinman, J. P. (1989). Hydrogen Tunneling in Enzyme Reactions. Science, 243, 1325-1330. https://doi.org/10.1126/science.2646716
Chung, M. K., Lee, H., & Caterina, M. J. (2003). Warm Temperatures Activate TRPV4 in Mouse 308 Keratinocytes. The Journal of Biological Chemistry, 278, 32037-32046. https://doi.org/10.1074/jbc.M303251200
Deing, V., Roggenkamp, D., Kühnl, J., Gruschka, A., Stäb, F., Wenck, H. et al. (2013). Oxytocin Modulates Proliferation and Stress Responses of Human Skin Cells: Implications for Atopic Dermatitis. Experimental Dermatology, 22, 399-405. https://doi.org/10.1111/exd.12155
Denda, M. (2011). Effects of Topical Application of Aqueous Solutions of Hexoses on Epidermal Permeability Barrier Recovery Rate after Barrier Disruption. Experimental Dermatology, 20, 943-944. https://doi.org/10.1111/j.1600-0625.2011.01329.x
Denda, M. (2016). Sensing Environmental Factors: The Emerging Role of Receptors in Epidermal Homeostasis and Whole Body Health. In G. T. Wondrak (Ed.), Skin Stress Response Pathways: Environmental Factors and Molecular Opportunities (pp. 403-414). Cham: Springer. https://doi.org/10.1007/978-3-319-43157-4_19
Denda, M., & Denda, S. (2007). Air-Exposed Keratinocytes Exhibited Intracellular Oscillation. Skin Research and Technology, 13, 195-201. https://doi.org/10.1111/j.1600-0846.2007.00210.x
Denda, M., & Fuziwara, S. (2008). Visible Radiation Affects Epidermal Permeability Barrier Recovery: Selective Effects of Red and Blue Light. Journal of Investigative Dermatology, 128, 1335-1336. https://doi.org/10.1038/sj.jid.5701168
Denda, M., & Kumazawa, N. (2010). Effects of Metals on Skin Permeability Barrier Recovery. Experimental Dermatology, 19, e124-e127. https://doi.org/10.1111/j.1600-0625.2009.01015.x
Denda, M., & Nakatani, M. (2010). Acceleration of Permeability Barrier Recovery by Exposure of Skin to 10-30 Kilohertz Sound. British Journal of Dermatology, 162, 503-507. https://doi.org/10.1111/j.1365-2133.2009.09509.x
Denda, M., & Tsutsumi, M. (2014). Possible Role of Epidermal Keratinocytes in the Construction of Acupuncture Meridians. Journal of Acupuncture and Meridian Studies, 7, 92-94. https://doi.org/10.1016/j.jams.2013.03.002
Denda, M., Denda, S., Tsutsumi, M., Goto, M., Kumamoto, J., Nakatani, M. et al. (2014). Frontiers in Epidermal Barrier Homeostasis—An Approach to Mathematical Modeling of Epidermal Calcium Dynamics. Experimental Dermatology, 23, 79-82. https://doi.org/10.1111/exd.12302
Denda, M., Fuziwara, S., & Hibino, T. (2006). Expression of Voltage-Gated Calcium Channel Subunit αC1 in Epidermal Keratinocytes and Effects of Agonist and Antagonists of the Channel on Skin Barrier Homeostasis. Experimental Dermatology, 15, 455-460. https://doi.org/10.1111/j.0906-6705.2006.00430.x
Denda, M., Fuziwara, S., & Inoue, K. (2003a). Beta-2-Adrenergic Receptor Antagonist Accelerates Skin Barrier Recovery and Reduces Epidermal Hyperplasia Induced by Barrier Disruption. Journal of Investigative Dermatology, 121, 142-148. https://doi.org/10.1046/j.1523-1747.2003.12310.x
Denda, M., Fuziwara, S., & Inoue, K. (2003b). Influx of Calcium and Chloride Ions into Epidermal Keratinocytes Regulates Exocytosis of Epidermal Lamellar Bodies and Skin Permeability Barrier Homeostasis. Journal of Investigative Dermatology, 121, 362-367. https://doi.org/10.1046/j.1523-1747.2003.12367.x
Denda, M., Fuziwara, S., Inoue, K. (2004). Association of Cyclic AMP with Permeability Barrier Homeostasis. Journal of Investigative Dermatology, 122, 140-146. https://doi.org/10.1046/j.0022-202X.2003.22115.x
Denda, M., Inoue, K., Fuziwara, S., & Denda, S. (2002a). P2X Purinergic Receptor Antagonist Accelerates Skin Barrier Repair and Prevents Epidermal Hyperplasia Induced by Skin Barrier Disruption. Journal of Investigative Dermatology, 119, 1034-1040. https://doi.org/10.1046/j.1523-1747.2002.19505.x
Denda, M., Inoue, K., Inomata, S., & Denda, S. (2002b). GABA (A) Receptor Agonists Accelerate Cutaneous Barrier Recovery and Prevent Epidermal Hyperplasia Induced by Barrier Disruption. Journal of Investigative Dermatology, 119, 1041-1047. https://doi.org/10.1046/j.1523-1747.2002.19504.x
Denda, M., Menon, G. K., & Elias, P. M. (2018). Did Hairlessness Stimulate an Increase in Hominin Brain Size? Insight from Cutaneous Neurosensory Interface and Comparative Vertebrate Morphology. Anthropology, 6, 1000199-1000199. https://doi.org/10.4172/2332-0915.1000199
Denda, M., Tsutsumi, M., & Denda, S. (2010). Topical Application of TRPM8 Agonists Accelerates Skin Permeability Barrier Recovery and Reduces Epidermal Proliferation Induced by Barrier Insult: The Role of Cold-Sensitive TRP Receptors in Epidermal Permeability Barrier Homeostasis. Experimental Dermatology, 19, 791-795. https://doi.org/10.1111/j.1600-0625.2010.01154.x
Denda, S., Takei, K., Kumamoto, J., Goto, M., Tsutsumi, M., & Denda, M. (2012). Oxytocin Is Expressed in Epidermal Keratinocytes and Released upon Stimulation with Adenosine 5’-[Gamma-Thio] Triphosphate in Vitro. Experimental Dermatology, 21, 535-537. https://doi.org/10.1111/j.1600-0625.2012.01507.x
Eddington, A. S. (2011). The Crucial Phenomena. In A. S. Eddington (Ed), Report on the Relativity Theory of Gravitation the Physical Society of London (pp. 48-58). London, UK: Forgotten Bools.
Einstein, A. (1911). über den Einfluß der Schwerkraft auf die Ausbreitung des Lichtes. Annalen der Physik (Leipzig), 340, 898-908. https://doi.org/10.1002/andp.19113401005
Fuziwara, S., Inoue, K., & Denda, M. (2003). NMDA-Type Glutamate Receptor Is Associated with Cutaneous Barrier Homeostasis. Journal of Investigative Dermatology, 120, 1023-1029. https://doi.org/10.1046/j.1523-1747.2003.12238.x
Fuziwara, S., Suzuki, A., Inoue, K., & Denda, M. (2005). Dopamine D2-Like Receptor Agonists Accelerate Barrier Repair and Inhibit the Epidermal Hyperplasia Induced by Barrier Disruption. Journal of Investigative Dermatology, 125, 783-789. https://doi.org/10.1111/j.0022-202X.2005.23873.x
Giszter, S. F., McIntyre, J., & Bizzi, E. (1989). Kinematic Strategies and Sensorimotor Transformations in the Wiping Movements of Frogs. Journal of Neurophysiology, 62, 750-767. https://doi.org/10.1152/jn.1989.62.3.750
Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Stenzel, U., Kircher, M. et al. (2010). A Draft Sequence of the Neandertal Genome. Science, 328, 710-722. https://doi.org/10.1126/science.1188021
Hanlon, R. T., Maxwell, M. R., Shashar N., Loew, E. R., & Boyle, K. L. (1999). An ethogram of Body Patterning Behavior in the Biomedically and Commercially Valuable Squid Loligo pealei off Cape Cod, Massachusetts. The Biological Bulletin, 19, 49-62. https://doi.org/10.2307/1542996
Hochner, B. (2012). An Embodied View of Octopus Neurobiology. Current Biology, 22, R887-R892. https://doi.org/10.1016/j.cub.2012.09.001
Hochner, B. (2013). How Nervous Systems Evolve in Relation to Their Embodiment: What We Can Learn from Octopuses and Other Molluscs. Brain, Behavior and Evolution, 82, 19-30. https://doi.org/10.1159/000353419
Huber, M., Siegenthaler, G., Mirancea, N., Marenholz, I., Nizetic, D., Breitkreutz, D. et al. (2005). Isolation and Characterization of Human Repetin, a Member of the Fused Gene Family of the Epidermal Differentiation Complex. Journal of Investigative Dermatology, 124, 998-1007. https://doi.org/10.1111/j.0022-202X.2005.23675.x
Ikeyama, K., Fuziwara, S., & Denda, M. (2007). Topical Application of Neuronal Nitric Oxide Synthase Inhibitor Accelerates Cutaneous Barrier Recovery and Prevents Epidermal Hyperplasia Induced by Barrier Disruption. Journal of Investigative Dermatology, 127, 1713-1719. https://doi.org/10.1038/sj.jid.5700742
Ikeyama, K., Nakatani, M., Kumamoto, J., & Denda, M. (2013). Distinct Intracellular Calcium Responses of Individual Cultured Human Keratinocytes to Air Pressure Changes. Skin Research and Technology, 19, 346-351. https://doi.org/10.1111/srt.12045
Inoue, K., Denda, M., Tozaki, H., Fujishita, K., Koizumi, S., & Inoue, K. (2005). Characterization of Multiple P2X Receptors in Cultured Normal Human Epidermal Keratinocytes. Journal of Investigative Dermatology, 124, 756-763. https://doi.org/10.1111/j.0022-202X.2005.23683.x
Inoue, K., Koizumi, S., Fuziwara, S., Denda, S., Inoue, K., & Denda, M. (2002). Functional Vanilloid Receptors in Cultured Normal Human Keratinocytes. Biochemical and Biophysical Research Communications, 291, 124-129. https://doi.org/10.1006/bbrc.2002.6393
Inoue, K., Takei, K., & Denda, M. (2015). Functional Glycine Receptor in Cultured Human Keratinocytes. Experimental Dermatology, 24, 307-309. https://doi.org/10.1111/exd.12651
Kitamura, T., Ogawa, S. K., Roy, D. S., Okuyama, T., Morrissey, M. D. et al. (2017). Engrams and Circuits Crucial for Systems Consolidation of a Memory. Science, 356, 73-78. https://doi.org/10.1126/science.aam6808
Kobayashi, Y., & Nagayama, M. (2016). Mathematical Model of Epidermal Structure. In R. S. Anderssen et al. (Eds.), Applications + Practical Conceptualization +Mathematics = Fruitful Innovation, Mathematics for Industry (Vol. 11, pp. 121-126). Tokyo, Japan: Springer. https://doi.org/10.1007/978-4-431-55342-7_11
Kobayashi, Y., Sanno, Y., Sakai, A., Sawabu, Y., Tustsumi, M., Goto, M. et al. (2014). Mathematical Modeling of Calcium Waves Induced by Mechanical Stimulation in Keratinocytes. PLoS ONE, 9, e92650. https://doi.org/10.1371/journal.pone.0092650
Kobayashi, Y., Sawabu, Y., Kitahata, H., Denda, M., & Nagayama, M. (2016). Mathematical Model for Calcium-Assisted Epidermal Homeostasis. Journal of Theoretical Biology, 397, 52-60. https://doi.org/10.1016/j.jtbi.2016.02.032
Kumamoto, J., Nakanishi, S., Makita, M., Uesaka, M., Yasugahira, Y., Kobayashi, Y. et al. (2018). Mathematical-Model-Guided Development of Full-Thickness Epidermal Equivalent. Scientific Reports, 8, 17999. https://doi.org/10.1038/s41598-018-36647-y
Kverková, K., Bělíková, T., Olkowicz, S., Pavelková, Z., O’Riain, M. J., Šumbera, R., Burda, H., Bennett, N. C., & Němec, P. (2018). Sociality Does Not Drive the Evolution of Large Brains in Eusocial African Mole-Rats. Scientific Reports, 8, 9203. https://doi.org/10.1038/s41598-018-26062-8
Lattes, C. M. G., Muirhead, H., Occhialini, G. P. S., & Powell, C. F. (1947). Processes Involving Charged Mesons. Nature, 159, 694-697. https://doi.org/10.1038/159694a0
Liedtke, W. (2007). Role of TRPV Ion Channels in Sensory Transduction of Osmotic Stimuli in Mammals. Experimental Physiology, 92, 507-512. https://doi.org/10.1113/expphysiol.2006.035642
Lisi, A., Foletti, A., Ledda, M., Rosola, E., Giuliani, L., D’Emilia, E., & Grimaldi, S. (2006). Extremely Low Frequency 7 Hz 100 microT Electromagnetic Radiation Promotes Differentiation in the Human Epithelial Cell Line HaCaT. Electromagnetic Biology and Medicine, 25, 269-280. https://doi.org/10.1080/15368370601044184
Lyras, G. A. (2018). Brain Changes during Phyletic Dwarfing in Elephants and Hippos. Brain, Behavior and Evolution, 92, 167-181. https://doi.org/10.1159/000497268
Menzel, R. (2012). The Honeybee as a Model for Understanding the Basis of Cognition. Nature Reviews, 13, 758-768. https://doi.org/10.1038/nrn3357
Mischiati, M., Lin, H. T., Herold, P., Imler, E., Olberg, R., & Leonardo, A. (2015). Internal Models Direct Dragonfly Interception Steering. Nature, 517, 333-338. https://doi.org/10.1038/nature14045
Moehring, F., Cowie, A. M., Menzel, A. D., Weyer, A. D., Grzybowski, M., T., Arzua, T. et al. (2018). Keratinocytes Mediate Innocuous and Noxious Touch via ATP-P2X4 Signaling. eLife, 7, e31684. https://doi.org/10.7554/eLife.31684
Nakatani, M., Kawasoe, T., & Denda, M. (2011). Sex Difference in Human Fingertip Recognition of Micron-Level Randomness as Unpleasant. International Journal of Cosmetic Science, 33, 346-350. https://doi.org/10.1111/j.1468-2494.2010.00634.x
Nilsson, G. (1996). Brain and Body Oxygen Requirements of Gnathonemus petersii, a Fish with an Exceptionally Large Brain. Journal of Experimental Biology, 199, 603-607.
Packard, A. (1972). Cephalopods and Fish: The Limit of Convergence. Biological Reviews, 47, 241-307. https://doi.org/10.1111/j.1469-185X.1972.tb00975.x
Paladini, R. D., Takahashi, K., Bravo, N. S., & Coulombe, P. A. (1996). Onset of Re-Epithelialization after Skin Injury Correlates with a Reorganization of Keratin Filaments in Wound Edge Keratinocytes: Defining a Potential Role for Keratin 16. The Journal of Cell Biology, 132, 381-397. https://doi.org/10.1083/jcb.132.3.381
Pang, Z., Sakamoto, T., Tiwari, V., Kim, Y. S., Yang, F., Dong, X. et al. (2015). Selective Keratinocyte Stimulation Is Sufficient to Evoke Nociception in Mice. Pain, 156, 656-665. https://doi.org/10.1097/j.pain.0000000000000092
Pauli, W. (2012). The Influence of Archetypal Ideas on Kepler’s Theories. In C. G. Jung, & W. Pauli (Eds.), The Interpretation of Nature and the Psych (pp. 152). New York: Ishi Press.
Peier, A. M., Reeve, A. J., Andersson, D. A., Moqrich, A., Earley, T. J., Hergarden A. C. et al. (2002). A Heat-Sensitive TRP Channel Expressed in Keratinocytes. Science, 296, 2046-2049. https://doi.org/10.1126/science.1073140
Pruszynski, J. A., & Johansson, R. S. (2014). Edge-Orientation Processing in First-Order Tactile Neurons. Nature Neuroscience, 17, 1404-1409. https://doi.org/10.1038/nn.3804
Roberts, P., & Stewart, B. A. (2018). Defining the ‘Generalist Specialist’ Niche for Pleistocene Homo sapiens. Nature Human Behaviour, 2, 542-550. https://doi.org/10.1038/s41562-018-0394-4
Slominski, A., Wortsman, J., Luger, T., Paus, R., & Solomon, S. (2000). Corticotropin Releasing Hormone and Proopiomelanocortin Involvement in the Cutaneous Response to Stress. Physiological Reviews, 80, 979-1020. https://doi.org/10.1152/physrev.2000.80.3.979
Slominski, A., Wortsman, J., Pisarchik, A., Zbytek, B., Linton, E. A., Mazurkiewicz, J. E., & Wei, E. T. (2001). Cutaneous Expression of Corticotropin-Releasing Hormone (CRH), Urocortin, and CRH Receptors. FASEB Journal, 15, 1678-1693. https://doi.org/10.1096/fj.00-0850rev
Spikins, P., Wright, B., & Hodgson, D. (2016). Are There Alternative Adaptive Strategies to Human Pro-Sociality? The Role of Collaborative Morality in the Emergence of Personality Variation and Autistic Traits. Time & Mind, 9, 289-313. https://doi.org/10.1080/1751696X.2016.1244949
Stojadinovic, O., Sawaya, A., Pastar, I., & Tomic-Canic, M. (2013). Glucocorticoid Receptor Localizes to Adherens Junctions at the Plasma Membrane of Keratinocytes. PLoS ONE, 30, e63453. https://doi.org/10.1371/journal.pone.0063453
Takei, K., Denda, S., Kumamoto, J., & Denda, M. (2013). Low Environmental Humidity Induces Synthesis and Release of Cortisol in an Epidermal Organotypic Culture System. Experimental Dermatology, 22, 662-664. https://doi.org/10.1111/exd.12224
Tsutsumi, M., Denda, S., Ikeyama, K., Goto, M., & Denda, M. (2010a). Exposure to Low Temperature Induces Elevation of Intracellular Calcium in Cultured Human Keratinocytes. Journal of Investigative Dermatology, 130, 1945-1948. https://doi.org/10.1038/jid.2010.33
Tsutsumi, M., Goto, M., & Denda M. (2013). Dynamics of Intracellular Calcium in Cultured Human Keratinocytes after Localized Cell Damage. Experimental Dermatology, 22, 367-369. https://doi.org/10.1111/exd.12136
Tsutsumi, M., Goto, M., Denda, S., & Denda, M. (2011a). Morphological and Functional Differences in Co-Culture System of Keratinocytes and Dorsal Root Ganglion-Derived Cells Depending on Time of Seeding. Experimental Dermatology, 20, 464-467. https://doi.org/10.1111/j.1600-0625.2011.01276.x
Tsutsumi, M., Ikeyama, K., Denda, S., Nakanishi, J., Fuziwara, S., Aoki, H., & Denda, M. (2009a). Expressions of Rod and Cone Photoreceptor-Like Proteins in Human Epidermis. Experimental Dermatology, 18, 567-570. https://doi.org/10.1111/j.1600-0625.2009.00851.x
Tsutsumi, M., Kitahata, H., Fukuda, M., Kumamoto, J., Goto, M., Denda, S. et al. (2016). Numerical and Comparative Three-Dimensional Structural Analysis of Peripheral Nerve Fibers in Epidermis of Atopic Dermatitis Patients. British Journal of Dermatology, 174, 191-194. https://doi.org/10.1111/bjd.13974
Tsutsumi, M., Kitahata, H., Nakata, S., Sanno, Y., Nagayama, M., & Denda, M. (2010b). Mathematical Analysis of Intercellular Calcium Propagation Induced by ATP. Skin Research and Technology, 16, 146-150. https://doi.org/10.1111/j.1600-0846.2009.00420.x
Tsutsumi, M., Kumamoto, J., & Denda, M. (2011b). Intracellular Calcium Response to High Temperatureis Similar in Undifferentiated and Differentiated Cultured Human Keratinocytes. Experimental Dermatology, 20, 839-840. https://doi.org/10.1111/j.1600-0625.2011.01318.x
Tsutusmi, M., Inoue, K., Denda, S., Ikeyama, K., Goto, M., & Denda, M. (2009b). Mechanical-Stimulation-Evoked Calcium Waves in Proliferating and Differentiated Human Keratinocytes. Cell and Tissue Research, 338, 99-106. https://doi.org/10.1007/s00441-009-0848-0
von der Emde, G., Schwarz, S., Gomez, L., Budelli, R., & Grant K. (1998). Electric Fish Measure Distance in the Dark. Nature, 395, 890-894. https://doi.org/10.1038/27655
Wakamatsu, K., Graham, A., Cook, D., & Thody, A. J. (1997). Characterization of ACTH Peptides in Human Skin and Their Activation of the Melanocortin-1 Receptor. Pigment Cell Research, 10, 288-297. https://doi.org/10.1111/j.1600-0749.1997.tb00688.x
Xu, H., Delling, M., Jun, J. C., & Clapham, D. E. (2006). Oregano, Thyme and Clove-Derived Flavors and Skin Sensitizers Activate Specific TRP Channels. Nature Neuroscience, 9, 628-635. https://doi.org/10.1038/nn1692
Yukawa, H. (1935). On the Interaction of Elementary Particles. I. Proceedings of the Physico-Mathematical Society of Japan, 17, 48-57.