тел. +38 (044) 483-12-82

№5(6) 2023

Eng

DOI 10.37219/2528-8253-2023-5-76

Медведєв ВВ, Косаковський АЛ

МОЛЕКУЛЯРНІ МЕХАНІЗМИ ОНТОГЕНЕЗУ ЗАВИТКИ: КОРОТКИЙ ОГЛЯД

Медведєв Володимир Вікторович
Національний медичний університет імені О.О. Богомольця
Професор кафедри нейрохірургії
доктор медичних наук, професор
Email: vavo2010@gmail.com
ORCID ID: https://orcid.org/0000-0001-7236-3191
Scopus Author ID: 57195130399
ResearcherID: P-7278-2018
Loop profile: 770935
ResearcherID: P-7278-2018

Косаковський Анатолій Лук’янович
Національний університет охорони здоров’я України ім. П.Л. Шупика
Кафедра оториноларингології, дитячої оториноларингології та сурдології
Доктор медичних наук, професор
E-mail: akosakovskyi@gmail.com
ORCID ID: 0000-0001-7194-420X

Анотація

Будова органу слуху дивує драматичним поєднанням простоти і ємкості, хвилює несподіваністю рішень і залишається у багатьох питаннях предметом активного наукового пошуку. Поза сумнівом, онтогенез такого вишуканого механізму непростий і на даний час накопичено товстий масив даних щодо молекулярної регуляції цього процесу. Технологічний інструментарій сьогочасної біомедичної науки дозволяє не лише вивчати, а й працювати на молекулярно-генетичному рівні і з окремими незрілими клітинами. Отже, оглянуті у цій статті дані мають, окрім очевидного фундаментального, ще й істотне прикладне значення, оскільки наближають вирішення основної проблеми аудіології – відсутність відновлення популяції слухових клітин-рецепторів, тобто, відновлення слуху.

Ключові слова: завитка, спіральний орган, волоскові клітини, спіральний ганглій, тонотопія, онтогенез внутрішнього вуха.

Завантажити .PDF

Література

  1. Gage NM, Baars BJ, editors. Fundamentals of Cognitive Neuroscience. Second Edition. Academic Press; 2018. Chapter 5, Sound, Speech, and Music Perception; p. 143-84. https://doi.org/10.1016/B978-0-12-803813-0.00005-2.
  2. KandlerK, editor. The Oxford Handbook of the Auditory Brainstem. Oxford University Press; 2018. Chapter 26, Kraus N, Nicol T. Brainstem Encoding of Speech and Music Sounds in Humans; p. 741-758. https://doi.org/10.1093/oxfordhb/9780190849061.013.26.
  3. Olusanya BO, Davis AC, Hoffman HJ. Hearing loss: rising prevalence and impact. Bull World Health Organ. 2019 Oct 1;97(10):646-646A. doi: 10.2471/BLT.19.224683.
  4. Zahara D, Dewi RD, Aboet A, Putranto FM, Lubis ND, Ashar T. Variations in Cochlear Size of Cochlear Implant Candidates. Int Arch Otorhinolaryngol. 2019 Apr;23(2):184-190. doi: 10.1055/s-0038-1661360.
  5. Hrncirik F, Roberts I, Sevgili I, Swords C, Bance M. Models of Cochlea Used in Cochlear Implant Research: A Review. Ann Biomed Eng. 2023 Jul; 51 (7):1390-1407. doi: 10.1007/s10439-023-03192-3.
  6. Spiegel JL, Polterauer D, Hempel JM, Canis M, Spiro JE, Müller J. Variation of the cochlear anatomy and cochlea duct length: analysis with a new tablet-based software. Eur Arch Otorhinolaryngol. 2022 Apr;279(4):1851-1861. doi: 10.1007/s00405-021-06889-0.
  7. Hatton IA, Galbraith ED, Merleau NSC, Miettinen TP, Smith BM, Shander JA. The human cell count and size distribution. Proc Natl Acad Sci USA. 2023 Sep 26;120(39):e2303077120. doi: 10.1073/pnas.2303077120.
  8. McPherson DR. Sensory Hair Cells: An Introduction to Structure and Physiology. Integr Comp Biol. 2018 Aug 1;58(2):282-300. doi: 10.1093/icb/icy064.
  9. Fettiplace R. Hair Cell Transduction, Tuning, and Synaptic Transmission in the Mammalian Cochlea. Compr Physiol. 2017 Sep 12;7(4):1197-1227. doi: 10.1002/cphy.c160049.
  10. Miller KK, Atkinson P, Mendoza KR, Ó Maoiléidigh D, Grillet N. Dimensions of a Living Cochlear Hair Bundle. Front Cell Dev Biol. 2021 Nov 25;9:742529. doi: 10.3389/fcell.2021.742529.
  11. Wright A. Scanning electron microscopy of the human cochlea – the organ of Corti. Arch Otorhinolaryngol. 1981;230(1):11-9. doi: 10.1007/BF00665375.
  12. Ulehlová L, Voldrich L, Janisch R. Correlative study of sensory cell density and cochlear length in humans. Hear Res. 1987;28(2-3):149-51. doi: 10.1016/0378-5955(87)90045-1.
  13. Carricondo F, Romero-Gómez B. The Cochlear Spiral Ganglion Neurons: The Auditory Portion of the VIII Nerve. Anat Rec (Hoboken). 2019 Mar; 302(3):463-471. doi: 10.1002/ar.23815.
  14. Frank MM, Goodrich LV. Talking back: Development of the olivocochlear efferent system. Wiley Interdiscip Rev Dev Biol. 2018 Nov; 7(6):e324. doi: 10.1002/wdev.324.
  15. Spoendlin H, Schrott A. Analysis of the human auditory nerve. Hear Res. 1989 Dec;43(1):25-38. doi: 10.1016/0378-5955(89)90056-7.
  16. Zhang KD, Coate TM. Recent advances in the development and function of type II spiral ganglion neurons in the mammalian inner ear. Semin Cell Dev Biol. 2017 May;65:80-87. doi: 10.1016/j.semcdb.2016.09.017.
  17. Johnson SL, Safieddine S, Mustapha M, Marcotti W. Hair Cell Afferent Synapses: Function and Dysfunction. Cold Spring Harb Perspect Med. 2019 Dec 2;9(12):a033175. doi: 10.1101/cshperspect.a033175.
  18. Souffi S, Nodal FR, Bajo VM, Edeline JM. When and How Does the Auditory Cortex Influence Subcortical Auditory Structures? New Insights About the Roles of Descending Cortical Projections. Front Neurosci. 2021 Aug 3;15:690223. doi: 10.3389/fnins.2021.690223.
  19. Li J. Liquid-liquid phase separation in hair cell stereocilia development and maintenance. Comput Struct Biotechnol J. 2023 Feb 24;21:1738-1745. doi: 10.1016/j.csbj.2023.02.040.
  20. Bazard P, Frisina RD, Acosta AA, Dasgupta S, Bauer MA, Zhu X, Ding B. Roles of Key Ion Channels and Transport Proteins in Age-Related Hearing Loss. Int J Mol Sci. 2021 Jun 7;22(11):6158. doi: 10.3390/ijms22116158.
  21. Lipovsek M, Elgoyhen AB. The evolutionary tuning of hearing. Trends Neurosci. 2023 Feb;46 (2):110-123. doi: 10.1016/j.tins.2022.12.002.
  22. Effertz T, Moser T, Oliver D. Recent advances in cochlear hair cell nanophysiology: subcellular compartmentalization of electrical signaling in compact sensory cells. Fac Rev. 2020 Dec 21;9:24. doi: 10.12703/r/9-24.
  23. Berger J, Rubinstein J. A flexible anatomical set of mechanical models for the organ of Corti. R Soc Open Sci. 2021 Sep 15;8(9):210016. doi: 10.1098/rsos.210016.
  24. Lin CJ, Bozovic D. Effects of Efferent Activity on Hair Bundle Mechanics. J Neurosci. 2020 Mar 18; 40(12):2390-2402. doi: 10.1523/JNEUROSCI.1312-19.2020.
  25. Kandler K, Clause A, Noh J. Tonotopic reorganization of developing auditory brainstem circuits. Nat Neurosci. 2009 Jun;12(6):711-7. doi: 10.1038/nn.2332.
  26. Li H, Helpard L, Ekeroot J, Rohani SA, Zhu N, Rask-Andersen H, Ladak HM, Agrawal S. Three-dimensional tonotopic mapping of the human cochlea based on synchrotron radiation phase-contrast imaging. Sci Rep. 2021 Feb 24;11(1): 4437. doi: 10.1038/s41598-021-83225-w.
  27. Mann ZF, Kelley MW. Development of tonotopy in the auditory periphery. Hear Res. 2011 Jun; 276(1-2):2-15. doi: 10.1016/j.heares.2011.01.011.
  28. Basch ML, Brown RM 2nd, Jen HI, Groves AK. Where hearing starts: the development of the mammalian cochlea. J Anat. 2016 Feb;228(2):233-54. doi: 10.1111/joa.12314.
  29. Fettiplace R. Diverse Mechanisms of Sound Frequency Discrimination in the Vertebrate Cochlea. Trends Neurosci. 2020 Feb;43(2):88-102. doi: 10.1016/j.tins.2019.12.003.
  30. Brownell WE, Bader CR, Bertrand D, de Ribaupierre Y. Evoked mechanical responses of isolated cochlear outer hair cells. Science. 1985 Jan 11;227(4683):194-6. doi: 10.1126/science.3966153.
  31. Ashmore JF. A fast motile response in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier. J Physiol. 1987 Jul;388:323-47. doi: 10. 1113/jphysiol.1987.sp016617.
  32. National Research Council (US) Committee on Disability Determination for Individuals with Hearing Impairments; Dobie RA, Van Hemel S, editors. Hearing Loss: Determining Eligibility for Social Security Benefits. Washington (DC): National Academies Press (US); 2004. Chapter 2, Basics of Sound, the Ear, and Hearing. Available from: https://www.ncbi.nlm.nih.gov/books/NBK207834/
  33. Grocott T, Tambalo M, Streit A. The peripheral sensory nervous system in the vertebrate head: a gene regulatory perspective. Dev Biol. 2012 Oct 1;370(1):3-23. doi: 10.1016/j.ydbio.2012.06.028.
  34. Ladher RK. Changing shape and shaping change: Inducing the inner ear. Semin Cell Dev Biol. 2017 May;65:39-46. doi: 10.1016/j.semcdb.2016.10.006.
  35. Zine A, Fritzsch B. Early Steps towards Hearing: Placodes and Sensory Development. Int J Mol Sci. 2023 Apr 10;24(8):6994. doi: 10.3390/ijms24086994.
  36. Douceau S, Deutsch Guerrero T, Ferent J. Establishing Hedgehog Gradients during Neural Development. Cells. 2023 Jan 5;12(2):225. doi: 10.3390/cells12020225.
  37. Shin JO, Ankamreddy H, Jakka NM, Lee S, Kim UK, Bok J. Temporal and spatial expression patterns of Hedgehog receptors in the developing inner and middle ear. Int J Dev Biol. 2017;61(8-9):557-563. doi: 10.1387/ijdb.170155jb.
  38. Brown R, Groves AK. Hear, Hear for Notch: Control of Cell Fates in the Inner Ear by Notch Signaling. Biomolecules. 2020 Feb 28;10(3):370. doi: 10.3390/biom10030370.
  39. Zhou B, Lin W, Long Y, Yang Y, Zhang H, Wu K, Chu Q. Notch signaling pathway: architecture, disease, and therapeutics. Signal Transduct Target Ther. 2022 Mar 24;7(1):95. doi: 10.1038/s41392-022-00934-y.
  40. Stapornwongkul KS, Vincent JP. Generation of extracellular morphogen gradients: the case for diffusion. Nat Rev Genet. 2021 Jun;22(6):393-411. doi: 10.1038/s41576-021-00342-y.
  41. Simsek MF, Özbudak EM. Patterning principles of morphogen gradients. Open Biol. 2022 Oct; 12(10):220224. doi: 10.1098/rsob.220224.
  42. Gude F, Froese J, Manikowski D, Di Iorio D, Grad JN, Wegner S, Hoffmann D, Kennedy M, Richter RP, Steffes G, Grobe K. Hedgehog is relayed through dynamic heparan sulfate interactions to shape its gradient. Nat Commun. 2023 Feb 10; 14(1):758. doi: 10.1038/s41467-023-36450-y.
  43. Zhang Z, Zwick S, Loew E, Grimley JS, Ramanathan S. Mouse embryo geometry drives formation of robust signaling gradients through receptor localization. Nat Commun. 2019 Oct 4;10(1):4516. doi: 10.1038/s41467-019-12533-7.
  44. Boocock D, Hino N, Ruzickova N, Hirashima  T, Hannezo E. Theory of mechanochemical patterning and optimal migration in cell monolayers. Nat. Phys. 2021 Sep 28; 17, 267-74. doi: 10.1038/s41567-020-01037-7.
  45. Collinet C, Lecuit T. Programmed and self-organized flow of information during morphogenesis. Nat Rev Mol Cell Biol. 2021 Apr;22(4):245-265. doi: 10.1038/s41580-020-00318-6.
  46. Thompson MJ, Young CA, Munnamalai V, Umulis DM. Early radial positional information in the cochlea is optimized by a precise linear BMP gradient and enhanced by SOX2. Sci Rep. 2023 May 26;13(1):8567. doi: 10.1038/s41598-023-34725-4.
  47. de Celis JF, Bray S. Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development. 1997 Sep; 124(17):3241-51. doi: 10.1242/dev.124.17.3241.
  48. Elliott KL, Pavlinkova G, Chizhikov VV, Yamoah EN, Fritzsch B. Neurog1, Neurod1, and Atoh1 are essential for spiral ganglia, cochlear nuclei, and cochlear hair cell development. Fac Rev. 2021 May 11;10:47. doi: 10.12703/r/10-47.
  49. Dabdoub A, Fritzsch B, Popper A, Fay R, editors. The Primary Auditory Neurons of the Mammalian Cochlea. Springer, New York, NY; 2016. Goodrich LV. Early Development of the Spiral Ganglion, p. 11-48. https://doi.org/10.1007/978-1-4939-3031-9_2.
  50. Petitpré C, Faure L, Uhl P, Fontanet P, Filova I, Pavlinkova G, Adameyko I, Hadjab S, Lallemend F. Single-cell RNA-sequencing analysis of the developing mouse inner ear identifies molecular logic of auditory neuron diversification. Nat Commun. 2022 Jul 5;13(1):3878. doi: 10.1038/s41467-022-31580-1.
  51. Shrestha BR, Chia C, Wu L, Kujawa SG, Liberman MC, Goodrich LV. Sensory Neuron Diversity in the Inner Ear Is Shaped by Activity. Cell. 2018 Aug 23;174(5):1229-1246.e17. doi: 10.1016/j.cell.2018.07.007.
  52. Sanders TR, Kelley MW. Specification of neuronal subtypes in the spiral ganglion begins prior to birth in the mouse. Proc Natl Acad Sci U S A. 2022 Nov 29;119(48):e2203935119. doi: 10.1073/pnas.2203935119.
  53. Cohen R, Amir-Zilberstein L, Hersch M, Woland S, Loza O, Taiber S, Matsuzaki F, Bergmann S, Avraham KB, Sprinzak D. Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear. Nat Commun. 2020 Oct 12; 11(1):5137. doi: 10.1038/s41467-020-18894-8.
  54. Cohen R, Taiber S, Loza O, Kasirer S, Woland S, Sprinzak D. Precise alternating cellular pattern in the inner ear by coordinated hopping intercalations and delaminations. Sci Adv. 2023 Feb 22; 9(8):eadd2157. doi: 10.1126/sciadv.add2157.
  55. Webber JL, García-Añoveros J. Precision patterning: How inner hair cells “hop” to it. Sci Adv. 2023;9(8):eadg8662. doi: 10.1126/sciadv.adg8662.
  56. Tarchini B. A Reversal in Hair Cell Orientation Organizes Both the Auditory and Vestibular Organs. Front Neurosci. 2021 Sep 27;15:695914. doi: 10.3389/fnins.2021.695914.
  57. Coate TM, Scott MK, Gurjar M. Current concepts in cochlear ribbon synapse formation. Synapse. 2019 May;73(5):e22087. doi: 10.1002/syn.22087.
  58. Tani T, Koike-Tani M, Tran MT, Shribak M, Levic S. Postnatal structural development of mammalian Basilar Membrane provides anatomical basis for the maturation of tonotopic maps and frequency tuning. Sci Rep. 2021 Apr 7;11(1):7581. doi: 10.1038/s41598-021-87150-w.
  59. O’Sullivan JDB, Blacker TS, Scott C, Chang W, Ahmed M, Yianni V, Mann ZF. Gradients of glucose metabolism regulate morphogen signalling required for specifying tonotopic organisation in the chicken cochlea. Elife. 2023 Aug 4;12:e86233. doi: 10.7554/eLife.86233.
  60. Jeng JY, Ceriani F, Hendry A, Johnson SL, Yen P, Simmons DD, Kros CJ, Marcotti W. Hair cell maturation is differentially regulated along the tonotopic axis of the mammalian cochlea. J Physiol. 2020;598(1):151-170. doi: 10.1113/JP279012.
  61. Lahav A, Skoe E. An acoustic gap between the NICU and womb: a potential risk for compromised neuroplasticity of the auditory system in preterm infants. Front Neurosci. 2014 Dec 5;8:381. doi: 10.3389/fnins.2014.00381.
  62. Altoè A, Shera CA. The cochlear ear horn: geometric origin of tonotopic variations in auditory signal processing. Sci Rep. 2020 Nov 25; 10(1):20528. doi: 10.1038/s41598-020-77042-w.
  63. Cohen R, Sprinzak D. Mechanical forces shaping the development of the inner ear. Biophys J. 2021; 120(19):4142-4148. doi: 10.1016/j.bpj.2021.06.036.