Scanning thin-sheet laser imaging microscopy elucidates details on mouse ear development

Developmental Dynamics

Volumn 241, Issue 3, 2012, Pages 465-480

  Kopecky, Benjamin ^a,b   Johnson, Shane ^c   Schmitz, Heather ^c   Santi, Peter ^c   Fritzsch, Bernd ^a  

^a UNIVERSITY OF IOWA   (United States)

^b The University of Iowa   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Cochlea; Development; Ear; Endolymph; Perilymph; STSLIM

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL MATURATION; COCHLEA DUCT; CONTROLLED STUDY; EAR DEVELOPMENT; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GROWTH RATE; LASER MICROSCOPY; MALE; MORPHOGENESIS; MOUSE; NONHUMAN; ORGAN SIZE; ORGANOGENESIS; PRIORITY JOURNAL; SACCULUS; SOMATOSENSORY CORTEX; THIN SHEET LASER IMAGING MICROSCOPY; THREE DIMENSIONAL IMAGING; VESTIBULOCOCHLEAR NERVE;

ANIMALS; COCHLEA; EAR, INNER; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MORPHOGENESIS;

MAMMALIA; MURINAE;

EID: 84857046492     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23736     Document Type: Article

References (51)

1. Appler JM, Goodrich LV. 2011. Connecting the ear to the brain: molecular mechanisms of auditory circuit assembly. Prog Neurobiol 93: 488-508.
2. Berlanga ML, Phan S, Bushong EA, Wu S, Kwon O, Phung BS, Lamont S, Terada M, Tasdizen T, Martone ME, Ellisman MH. 2011. Three-dimensional reconstruction of serial mouse brain sections: solution for flattening high-resolution large-scale mosaics. Front Neuroanat 5: 17.
3. Bever MM, Fekete DM. 2002. Atlas of the developing inner ear in zebrafish. Dev Dyn 223: 536-543.
4. Bever MM, Jean YY, Fekete DM. 2003. Three-dimensional morphology of inner ear development in Xenopus laevis. Dev Dyn 227: 422-430.
5. Bouchard M, de Caprona D, Busslinger M, Xu P, Fritzsch B. 2010. Pax2 and Pax8 cooperate in mouse inner ear morphogenesis and innervation. BMC Dev Biol 10: 89.
6. Brigande JV, Kiernan AE, Gao X, Iten LE, Fekete DM. 2000. Molecular genetics of pattern formation in the inner ear: do compartment boundaries play a role? Proc Natl Acad Sci U S A 97: 11700-11706.
7. Cantos R, Cole LK, Acampora D, Simeone A, Wu DK. 2000. Patterning of the mammalian cochlea. Proc Natl Acad Sci U S A 97: 11707-11713.
8. Cross SH, McKie L, West K, Coghill EL, Favor J, Bhattacharya S, Brown SD, Jackson IJ. 2011. The Opdc missense mutation of Pax2 has a milder than loss-of-function phenotype. Hum Mol Genet 20: 223-234.
9. Fekete DM. 1999. Development of the vertebrate ear: insights from knockouts and mutants. Trends Neurosci 22: 263-269.
10. Fekete DM, Wu DK. 2002. Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol 12: 35-42.
11. Fritzsch B. 2003. Development of inner ear afferent connections: forming primary neurons and connecting them to the developing sensory epithelia. Brain Res Bull 60: 423-433.
12. Fritzsch B, Barald K, Lomax M. 1998. Early embryology of the vertebrate ear. In: Rubel EW, Popper AN, Fay RR, editors. Springer handbook of auditory research. Vol. XII. Development of the auditory system. New York: Springer Verlag. p 80-145.
13. Fritzsch B, Signore M, Simeone A. 2001. Otx1 null mutant mice show partial segregation of sensory epithelia comparable to lamprey ears. Dev Genes Evol 211: 388-396.
14. Glueckert R, Rask-Andersen H, Sergi C, Schmutzhard J, Mueller B, Beckmann F, Rittinger O, Hoefsloot LH, Schrott-Fischer A, Janecke AR. 2010. Histology and synchrotron radiation-based microtomography of the inner ear in a molecularly confirmed case of CHARGE syndrome. Am J Med Genet A 152A: 665-673.
15. Hama H, Kurokawa H, Kawano H, Ando R, Shimogori T, Noda H, Fukami K, Sakaue-Sawano A, Miyawaki A. 2011. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat Neurosci 30: 1481-1488.
16. Hulander M, Kiernan AE, Blomqvist SR, Carlsson P, Samuelsson EJ, Johansson BR, Steel KP, Enerback S. 2003. Lack of pendrin expression leads to deafness and expansion of the endolymphatic compartment in inner ears of Foxi1 null mutant mice. Development 130: 2013-2025.
17. Hurd EA, Adams ME, Layman WS, Swiderski DL, Beyer LA, Halsey KE, Benson JM, Gong TW, Dolan DF, Raphael Y, Martin DM. 2011. Mature middle and inner ears express Chd7 and exhibit distinctive pathologies in a mouse model of CHARGE syndrome. Hear Res 282: 184-195.
18. Johnson SB, Schmitz HM, Santi PA. 2011. TSLIM imaging and a morphometric analysis of the mouse spiral ganglion. Hear Res 278: 34-42.
19. Kiernan AE, Xu J, Gridley T. 2006. The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genet 2: e4.
20. Kim HM, Wangemann P. 2010. Failure of fluid absorption in the endolymphatic sac initiates cochlear enlargement that leads to deafness in mice lacking pendrin expression. PLoS One 5: e14041.
21. Kopecky B, Santi P, Johnson S, Schmitz H, Fritzsch B. 2011. Conditional deletion of N-Myc disrupts neurosensory and non-sensory development of the ear. Dev Dyn 240: 1373-1390.
22. Luo ZX, Ruf I, Schultz JA, Martin T. 2011. Fossil evidence on evolution of inner ear cochlea in Jurassic mammals. Proc Biol Sci 278: 28-34.
23. Ma Q, Anderson DJ, Fritzsch B. 2000. Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. J Assoc Res Otolaryngol 1: 129-143.
24. Martin P, Swanson GJ. 1993. Descriptive and experimental analysis of the epithelial remodellings that control semicircular canal formation in the developing mouse inner ear. Dev Biol 159: 549-558.
25. Morris JK, Maklad A, Hansen LA, Feng F, Sorensen C, Lee KF, Macklin WB, Fritzsch B. 2006. A disorganized innervation of the inner ear persists in the absence of ErbB2. Brain Res 1091: 186-199.
26. Morsli H, Choo D, Ryan A, Johnson R, Wu DK. 1998. Development of the mouse inner ear and origin of its sensory organs. J Neurosci 18: 3327-3335.
27. Nichols DH, Pauley S, Jahan I, Beisel KW, Millen KJ, Fritzsch B. 2008. Lmx1a is required for segregation of sensory epithelia and normal ear histogenesis and morphogenesis. Cell Tissue Res 334: 339-358.
28. Ohyama T, Groves AK. 2004. Expression of mouse Foxi class genes in early craniofacial development. Dev Dyn 231: 640-646.
29. Pan N, Jahan I, Kersigo J, Kopecky B, Santi P, Johnson S, Schmitz H, Fritzsch B. 2011. Conditional deletion of Atoh1 using Pax2-Cre results in viable mice without differentiated cochlear hair cells that have lost most of the organ of Corti. Hear Res 275: 66-80.
30. Pauley S, Lai E, Fritzsch B. 2006. Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Dev Dyn 235: 2470-2482.
31. Rubel EW, Fritzsch B. 2002. Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25: 51-101.
32. Rueda J, Cantos R, Lim DJ. 1996. Tectorial membrane-organ of Corti relationship during cochlear development. Anat Embryol (Berl) 194: 501-514.
33. Santi PA. 2011. Light sheet fluorescence microscopy: a review. J Histochem Cytochem 59: 129-138.
34. Santi PA, Johnson SB, Hillenbrand M, GrandPre PZ, Glass TJ, Leger JR. 2009. Thin-sheet laser imaging microscopy for optical sectioning of thick tissues. Biotechniques 46: 287-294.
35. Schacht P, Johnson SB, Santi PA. 2010. Implementation of a continuous scanning procedure and a line scan camera for thin-sheet laser imaging microscopy. Biomed Opt Express 1: 598-609.
36. Schlosser G. 2010. Making senses development of vertebrate cranial placodes. Int Rev Cell Mol Biol 283: 129-234.
37. Schroter T, Johnson S, John K, Santi P. 2012. Scanning thin-sheet laser imaging microscopy (sTSLIM) with structured illumination and HiLo background rejection. J Biomed Opt 3: 170-177.
38. Seifert H, Roher U, Staszyk C, Angrisani N, Dziuba D, Meyer-Lindenberg A. 2011. Optimising μCT imaging of the middle and inner cat ear. Anat Histol Embryol [Epub ahead of print].
39. Soukup GA, Fritzsch B, Pierce ML, Weston MD, Jahan I, McManus MT, Harfe BD. 2009. Residual microRNA expression dictates the extent of inner ear development in conditional Dicer knockout mice. Dev Biol 328: 328-341.
40. Steinke H, Wolff W. 2001. A modified Spalteholz technique with preservation of the histology. Ann Anat 183: 91-95.
41. Streeter GL. 1906. On the development of the membranous labyrinth and the acoustic and facial nerves in the human embryo. Am J Anat 6: 139-165.
42. Streeter GL. 1917. The development of the scala tympani, scala vestibuli and perioticular cistern in the human embryo. Am J Anat 21: 299-320.
43. Sun S, Bauer C, Beichel R. 2011. Automated 3D Segmentation of lungs with lung cancer in CT data using a novel robust active shape model approach. IEEE Trans Med Imaging [Epub ahead of print].
44. Takumida M, Harada Y. 1984. Development of the utricular macula in the mouse. Arch Otorhinolaryngol 241: 9-15.
45. Takumida M, Harada Y, Tagashira N. 1986. Development of the crista ampullaris in the mouse. J Laryngol Otol 100: 759-763.
46. Torres M, Giraldez F. 1998. The development of the vertebrate inner ear. Mech Dev 71: 5-21.
47. Voie AH, Burns DH, Spelman FA. 1993. Orthogonal-plane fluorescence optical sectioning: three-dimensional imaging of macroscopic biological specimens. J Microsc 170: 229-236.
48. Wilson JT. 1924. On the application of the Spalteholtz clearing method to the study of thick serial sections of embryos, with demonstration of specimens. J Anat 58: 101-104.
49. Yang T, Kersigo J, Jahan I, Pan N, Fritzsch B. 2011. The molecular basis of making spiral ganglion neurons and connecting them to hair cells of the organ of Corti. Hear Res 278: 21-33.
50. Yasuda M, Yamada S, Uwabe C, Shiota K, Yasuda Y. 2007. Three-dimensional analysis of inner ear development in human embryos. Anat Sci Int 82: 156-163.
51. Zou D, Erickson C, Kim EH, Jin D, Fritzsch B, Xu PX. 2008. Eya1 gene dosage critically affects the development of sensory epithelia in the mammalian inner ear. Hum Mol Genet 17: 3340-3356.