Immunohistochemical Characterization of Human Olfactory Tissue

Overview

Journal Laryngoscope

Specialty Otorhinolaryngology

Date 2011 Jul 28

PMID 21792956

Citations 89

Authors

Eric H Holbrook

Enming Wu

William T Curry

Derrick T Lin

James E Schwob

Affiliations

Soon will be listed here.

Abstract

Objectives/hypothesis: The pathophysiology underlying human olfactory disorders is poorly understood because biopsying the olfactory epithelium (OE) can be unrepresentative and extensive immunohistochemical analysis is lacking. Autopsy tissue enriches our grasp of normal and abnormal olfactory immunohistology and guides the sampling of the OE by biopsy. Furthermore, a comparison of the molecular phenotype of olfactory epithelial cells between rodents and humans will improve our ability to correlate human histopathology with olfactory dysfunction.

Study Design: An immunohistochemical analysis of human olfactory tissue using a comprehensive battery of proven antibodies.

Methods: Human olfactory mucosa obtained from 21 autopsy specimens was analyzed with immunohistochemistry. The position and extent of olfactory mucosa was assayed by staining whole mounts (WMs) with neuronal markers. Sections of the OE were analyzed with an extensive group of antibodies directed against cytoskeletal proteins and transcription factors, as were surgical specimens from an esthesioneuroblastoma.

Results: Neuron-rich epithelium is always found inferior to the cribriform plate, even at advanced age, despite the interruptions in the neuroepithelial sheet caused by patchy respiratory metaplasia. The pattern of immunostaining with our antibody panel identifies two distinct types of basal cell progenitors in human OE similar to rodents. The panel also clarifies the complex composition of esthesioneuroblastoma.

Conclusions: The extent of human olfactory mucosa at autopsy can easily be delineated as a function of age and neurologic disease. The similarities in human versus rodent OE will enable us to translate knowledge from experimental animals to humans and will extend our understanding of human olfactory pathophysiology.

Citing Articles

Cystic fibrosis alters the structure of the olfactory epithelium and the expression of olfactory receptors affecting odor perception.

Caballero I, Mbouamboua Y, Weise S, Lopez-Galvez R, Couralet M, Fleurot I Sci Adv. 2025; 11(9):eads1568.

PMID: 40020072 PMC: 11870070. DOI: 10.1126/sciadv.ads1568.

Orexin-A increases the differentiation of human olfactory sensory neurons through orexin receptor type 1.

Chen Y, Young T, Wang Y, Huang C, Gao Y, Huang T Regen Ther. 2024; 26:1058-1068.

PMID: 39582799 PMC: 11585478. DOI: 10.1016/j.reth.2024.10.014.

Neuroimmune interactions in the olfactory epithelium: maintaining a sensory organ at an immune barrier interface.

Ullah M, Rowan N, Lane A Trends Immunol. 2024; 45(12):987-1000.

PMID: 39550314 PMC: 11624989. DOI: 10.1016/j.it.2024.10.005.

Visualizing the human olfactory projection and ancillary structures in a 3D reconstruction.

Low V, Lin C, Su S, Osanlouy M, Khan M, Safaei S Commun Biol. 2024; 7(1):1467.

PMID: 39516237 PMC: 11549439. DOI: 10.1038/s42003-024-07017-4.

Olfactory and gustatory chemical sensor systems in the African turquoise killifish: Insights from morphology.

Giaquinto D, Fonsatti E, Bortoletti M, Radaelli G, De Felice E, de Girolamo P Cell Tissue Res. 2024; 398(3):239-252.

PMID: 39432108 PMC: 11615025. DOI: 10.1007/s00441-024-03923-5.

References

Holbrook E, Leopold D, Schwob J . Abnormalities of axon growth in human olfactory mucosa. Laryngoscope. 2005; 115(12):2144-54. DOI: 10.1097/01.MLG.0000181493.83661.CE. View

Lindsell C, Boulter J, Disibio G, Gossler A, Weinmaster G . Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol Cell Neurosci. 1996; 8(1):14-27. DOI: 10.1006/mcne.1996.0040. View

Zigman J, Westermark G, LaMendola J, Boel E, Steiner D . Human G(olf) alpha: complementary deoxyribonucleic acid structure and expression in pancreatic islets and other tissues outside the olfactory neuroepithelium and central nervous system. Endocrinology. 1993; 133(6):2508-14. DOI: 10.1210/endo.133.6.8243272. View

Feng W, Kauer J, Adelman L, Talamo B . New structure, the "olfactory pit," in human olfactory mucosa. J Comp Neurol. 1997; 378(4):443-53. View

Paik S, Lehman M, Seiden A, Duncan H, Smith D . Human olfactory biopsy. The influence of age and receptor distribution. Arch Otolaryngol Head Neck Surg. 1992; 118(7):731-8. DOI: 10.1001/archotol.1992.01880070061012. View

Jones D, Reed R . Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science. 1989; 244(4906):790-5. DOI: 10.1126/science.2499043. View

Bourne T, Bellizzi A, Stelow E, Loy A, Levine P, Wick M . p63 Expression in olfactory neuroblastoma and other small cell tumors of the sinonasal tract. Am J Clin Pathol. 2008; 130(2):213-8. DOI: 10.1309/TEDD2FCWH8W0H4HA. View

Yamagishi M, Fujiwara M, Nakamura H . Olfactory mucosal findings and clinical course in patients with olfactory disorders following upper respiratory viral infection. Rhinology. 1994; 32(3):113-8. View

Yee K, Pribitkin E, Cowart B, Vainius A, Klock C, Rosen D . Neuropathology of the olfactory mucosa in chronic rhinosinusitis. Am J Rhinol Allergy. 2009; 24(2):110-20. PMC: 5903554. DOI: 10.2500/ajra.2010.24.3435. View

10.

Huard J, Youngentob S, Goldstein B, Luskin M, Schwob J . Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J Comp Neurol. 1998; 400(4):469-86. View

11.

Leopold D, Hummel T, Schwob J, Hong S, Knecht M, Kobal G . Anterior distribution of human olfactory epithelium. Laryngoscope. 2000; 110(3 Pt 1):417-21. DOI: 10.1097/00005537-200003000-00016. View

12.

Leung C, Coulombe P, Reed R . Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci. 2007; 10(6):720-6. DOI: 10.1038/nn1882. View

13.

NAESSEN R . The identification and topographical localisation of the olfactory epithelium in man and other mammals. Acta Otolaryngol. 1970; 70(1):51-7. DOI: 10.3109/00016487009181858. View

14.

Schwarting G, Gridley T, Henion T . Notch1 expression and ligand interactions in progenitor cells of the mouse olfactory epithelium. J Mol Histol. 2007; 38(6):543-53. DOI: 10.1007/s10735-007-9110-9. View

15.

Caggiano M, Kauer J, Hunter D . Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron. 1994; 13(2):339-52. DOI: 10.1016/0896-6273(94)90351-4. View

16.

Witt M, Bormann K, Gudziol V, Pehlke K, Barth K, Minovi A . Biopsies of olfactory epithelium in patients with Parkinson's disease. Mov Disord. 2009; 24(6):906-14. DOI: 10.1002/mds.22464. View

17.

Mhawech P, Berczy M, Assaly M, Herrmann F, Bouzourene H, Allal A . Human achaete-scute homologue (hASH1) mRNA level as a diagnostic marker to distinguish esthesioneuroblastoma from poorly differentiated tumors arising in the sinonasal tract. Am J Clin Pathol. 2004; 122(1):100-5. DOI: 10.1309/QD0K-9Q1J-BH6B-5GQQ. View

18.

Johnson E, Eller P, Jafek B . Protein gene product 9.5-like and calbindin-like immunoreactivity in the nasal respiratory mucosa of perinatal humans. Anat Rec. 1997; 247(1):38-45. DOI: 10.1002/(SICI)1097-0185(199701)247:1<38::AID-AR6>3.0.CO;2-B. View

19.

Hasegawa S, Yamagishi M, Nakano Y . Microscopic studies of human olfactory epithelia following traumatic anosmia. Arch Otorhinolaryngol. 1986; 243(2):112-6. DOI: 10.1007/BF00453761. View

20.

Hahn C, Han L, Rawson N, Mirza N, Borgmann-Winter K, Lenox R . In vivo and in vitro neurogenesis in human olfactory epithelium. J Comp Neurol. 2005; 483(2):154-63. DOI: 10.1002/cne.20424. View