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New Techniques for Biopsy and Culture of Human Olfactory Epithelial Neurons

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New Techniques for Biopsy and Culture of Human Olfactory Epithelial Neurons ORIGINAL ARTICLE New Techniques for Biopsy and Culture of Human Olfactory Epithelial Neurons Franc¸ois Fe´ron, PhD; Christopher Perry, MBBS; John J. McGrath, MBBS, PhD; Alan Mackay-Sim, PhD Objective: To improve the success of culturing olfac- lium in a biopsy specimen ranged from 30% to 76%, de- tory neurons from human nasal mucosa by investigat- pending on its location. The dorsoposterior regions of ing the intranasal distribution of the olfactory epithe- the nasal septum and the superior turbinate provided the lium and devising new techniques for growing human highest probability, but, surprisingly, olfactory epithe- olfactory epithelium in vitro. lium was also found anteriorly and ventrally on both sep- tum and turbinates. A new method of culturing the ol- Design: Ninety-sevenbiopsyspecimenswereobtainedfrom factory epithelium was devised. This slice culture 33 individuals, aged 21 to 74 years, collected from 6 regions technique improved the success rate for generating ol- of the nasal cavity. Each biopsy specimen was bisected, and factory neurons from 10% to 90%. 1 piece was processed for immunohistochemistry or elec- tron microscopy while the other piece was dissected fur- Conclusions: This study explains and overcomes most ther for explant culture. Four culture techniques were per- of the variability in the success in observing neurogen- formed,includingwholeexplantsandexplantedbiopsyslices. esis in cultures of adult human olfactory epithelium. The Five days after plating, neuronal differentiation was induced techniques presented here make the human olfactory epi- by means of a medium that contained basic fibroblast growth thelium a useful model for clinical research into certain factor. After another 5 days, cultures were processed for im- olfactory dysfunctions and a model for the causes of neu- munocytochemical analysis. rodevelopmental and neurodegenerative diseases. Results: The probability of finding olfactory epithe- Arch Otolaryngol Head Neck Surg. 1998;124:861-866 HE OLFACTORY epithelium is, trast, olfactory neurogenesis can be stud- in many ways, similar to the ied in living patients and controls. The neuroepithelium of the em- adult olfactory epithelium is therefore an bryonic neural tube. Within accessible source of neuronal tissue in adult olfactory epithelium which to observe the early stages of neu- Tare stem cells that retain the capacity to di- rogenesis and neuronal differentiation and vide and give rise to neuronal precursors the factors that control and regulate these that further divide and differentiate into ma- processes.4,6 ture sensory neurons.1-3 Olfactory neuro- Although Murrell et al4 demon- genesis also occurs in humans: we have strated the potential for the study of neu- shown that human olfactory epithelium re- rogenesis in human patients, there re- tains the capacity for neurogenesis and neu- main problems with the efficacy of the From the School of ronal differentiation at least until the age technique as applied to living patients, Biomolecular and Biomedical of 72 years and that this can be demon- compared with postmortem studies. When Science, Griffith University, strated in tissue collected up to 25 hours nasal biopsy specimens are collected from Nathan, Australia (Drs Fe´ron post mortem.4 Thus, the human olfactory subjects, it is ethically important to col- and Mackay-Sim); Department epithelium has the potential to be used as lect as little tissue as necessary and to avoid of Otolaryngology, Princess a tool to examine certain human disor- rebiopsy. It is therefore vital to maximize Alexandra Hospital, South ders resulting from abnormal develop- the efficacy of the culture technique. Brisbane, Australia (Drs Perry ment of the nervous system. In our previous study, only approxi- and McGrath); and Queensland Neurogenesis has been shown to oc- mately 50% of explants produced viable Centre for Schizophrenia 5 Research, Wolston Park cur in the brain of the adult mouse, but cultures (cultures with at least an out- Hospital, Wacol, Australia this is not confirmed in humans. In any growth of epithelial cells), and of these, (Drs Fe´ron, McGrath, and event, neurogenesis in adult human brain only about 50% produced neurons after Mackay-Sim). could only be studied post mortem. In con- stimulation with basic fibroblast growth ARCH OTOLARYNGOL HEAD NECK SURG/ VOL 124, AUG 1998 861 ©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 SUBJECTS AND METHODS methanol at − 20°C and processed for immunocytochemi- cal analysis. Alternatively, some explants were cultured by a dif- Human nasal mucosa was obtained by biopsy during rou- ferent technique. Instead of fibronectin-coated chamber tine nasal surgery with the patient under general anesthe- slides, some explants were grown on small pieces of fibro- sia, with the use of an ethmoid forceps (No. 8211.551; nectin-coated 0.4-µm nitrocellulose membrane (Milli- Richard Wolf Medical, Hoyland Medical, Camp Hill, Aus- pore, North Ryde, Australia) at the interface of air and me- tralia). Ninety-seven biopsy specimens were obtained from dium.10 The nitrocellulose membrane was placed on a 33 individuals (24 men and 9 women aged 21 to 74 years); transwell insert (Millipore) within a 6-well Costar plate of these, 10 had nasal abnormalities, such as polyps. The (Trace Biosciences, Tingalpa, Queensland, Australia). The patients were undergoing surgery for septoplasty or turbi- well was filled so that the medium just wetted the surface nectomy. All samples were obtained under a protocol ap- of the plastic membrane. With the methylene blue stain- proved by the ethics committees of the hospital and uni- ing used to orient the tissue, some explants were plated lu- versity involved. All biopsy tissues were obtained with the men side down, while others were plated lumen side up. informed consent of the patients, and the studies were car- These cultures were otherwise treated identically to those ried out in accordance with the guidelines of the National grown on chamber slides, except that, after fixation and Health and Medical Research Council of Australia. immunochemistry, the plastic membranes were mounted Six areas of collection were chosen: the dorsomedial and on slides before the coverslip was applied. dorsoposterior areas of the superior turbinate, the dorsoan- For electron microscopy, the tissue pieces were fixed terior and the ventroposterior areas of the middle turbi- for 2 hours in ice-cold fixative composed of 4% glutaral- nate, and the dorsomedial and the dorsoposterior areas of dehyde in 0.1-mol/L sodium cacodylate buffer (pH 7.4). the septum. The approximate location of each biopsy was Tissues were then washed in the same buffer, postfixed in noted and marked on standardized “maps” of the septum 1% osmium tetroxide, washed, dipped in uranyl acetate, and the medial face of the lateral wall of the nasal cavity. To and embedded in Spurr epoxy resin (ProSciTech, Queens- aid localization of specimens collected from the septum, ref- land). Ultrathin sections were cut, stained with uranyl ac- erence points to adjacent landmarks were noted. In some etate and lead citrate, and viewed on an electron micro- cases, the luminal surface of the nasal epithelium was stained scope. For immunhistochemistry, the tissue pieces were with methylene blue before collection to assist in orienta- fixed in Bouin fixative for 2 hours and washed in phosphate- tion of the excised pieces during explant culture. buffered saline (pH 7.4). The tissues were embedded in par- Biopsy specimens were placed on ice in Dulbecco modi- affin, sectioned at 4 µm, and laid on slides coated with 3- fied Eagle medium (Gibco-BRL, Gaithersburg, Md) supple- aminopropyltriethoxy-silane (Sigma, Castle Hill, New South mented with a serum supplement (Monomed, CSL, Mel- Wales, Australia). bourne, Australia), penicillin, streptomycin, gentamicin, and Immunochemistry was performed with peroxidase- nystatin (Gibco-BRL). After 1 to 2 hours the specimens were conjugated secondary antibodies (Sigma) with diamino- bisected: 1 piece was processed for immunohistochemis- benzidine as the chromogen. The following polyclonal or try or electron microscopy, and the other was dissected fur- monoclonal antibodies were used: anti–olfactory marker ther for explant culture. For culture, biopsy specimens were protein (goat polyclonal antibody, gift of Frank Margolis, cut into pieces of approximately 1 to 2 mm2 or, alterna- PhD, University of Maryland, Baltimore), anti–neuron- tively, sliced (200-µm thickness) by means of a McIlwain specific b-tubulin type III (mouse monoclonal antibody, tissue chopper (Mickle Laboratory Engineering Company Sigma), and anti–microtubule-associated protein 5 (mouse Ltd, Gomshall, Surrey, England) before being transferred monoclonal antibody, Sigma). Fixed cultures or deparaf- to fibronectin-coated glass chamber slides and cultured in finized sections were incubated overnight at 4°C followed the conditions above, as previously described.4,6 Five days by appropriate species-specific antibodies and peroxidase later the cultures were exposed to FGF2 (50 ng/mL; reagents. Extensive controls were used to exclude or de- Boehringer-Mannheim, South Brisbane, Queensland, termine the extent of nonspecific binding of secondary an- Australia). Another 5 days later, cultures were fixed in tibody and the presence of endogenous peroxidase. factor (FGF2).4 Thus, the combined probability of ob- opsy location and culture method not be misinterpreted serving
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