Skip to main content
SpringerLink
Log in

Neuronal influence on B and H human blood-group antigen expression in rat cochlear cultures

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The presence of B and H human blood-group antigens was analyzed by immunocytochemistry in rat cochleas developing either in vivo or in vitro. Developing animals, on embryonic day (E) 18 and postnatal day (P) 3, were used for in vivo studies. For in vitro studies, cochleas were removed at E18 and placed for 3 or 8 days in organotypic culture either directly or after partial spiral ganglion removal. Results from epithelial regions from cochleas developing in vivo were similar to those observed in corresponding areas of direct organotypic cultures where the innervation from spiral ganglion neurons was present. Antibodies to human blood group antigens, anti B and anti AB, selectively labeled hair cells. The intensity of labeling was weak at E18, but increased at P3 in vivo or after 3–8 days in organotypic culture. Anti H antibodies showed weak labeling of the apical surface of hair cells and other epithelial cells at E18; this labeling also increased at P3 or after 3–8 days in culture. In contrast, the non-innervated regions from organotypic cultures, where ganglia were partially removed, exhibited an epithelial disorganization and no hair cell labeling with any of the antibodies studied. The present findings suggest that human blood-group antigen expression on developing cochlear hair cells of rats may be related to afferent nerve fiber influence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Acheson A, Rutishauser U (1988) Neural cell adhesion molecule regulates cell contact-mediated changes in choline acetyltransferase activity of embryonic chick sympathetic neurons. J Cell Biol 106:479–486

    Google Scholar 

  • Acheson A, Thoenen H (1983) Cell contact-mediated regulation of tyrosine hydroxylase synthesis in cultured bovine adrenal chromaffin cells. J Cell Biol 97:925–928

    Google Scholar 

  • Astic L, Le Pendu J, Mollicone R, Saucier D, Oriol R (1989) Cellular expression of H and B antigens in the rat olfactory system during development. J Comp Neurol 289:386–394

    Google Scholar 

  • Black IB, Hendry IA, Iversen LL (1972) Effects of surgical decentralization and nerve growth factor on the maturation of adrenergic neurons in a mouse sympathetic ganglion. J Neurochem 19:1367–1377

    Google Scholar 

  • Cajal SR (1919) Acción neurotrópica de los epitelios (Algunos detalles sobre el mecanismo genético de las ramificaciones nerviosas intra-epiteliales, sensitivas y sensoriales). Trab Lab Invest Biol U Madrid 17:181–228

    Google Scholar 

  • Chou DK, Dodd J, Jessell TM, Costello CE, Jungalwala FB (1989) Identification of α-galactose (α-fucose)-asialo GM1 glycolipid expressed by subsets of rat dorsal root ganglion neurons. J Biol Chem 264:3409–3416

    Google Scholar 

  • Christie GA (1964) Developmental stages in somite and post-somite rat embryos, based on external appearance, and including some features of the macroscopic development of the oral cavity. J Morphol 114:263–286

    Google Scholar 

  • Dabelsteen E, Vedtofte P, Hakomori S, Young WW (1982) Carbohydrate chains specific for blood group antigens in differentiation of human oral epithelium. J Invest Dermatol 79:3–7

    Google Scholar 

  • Dabelsteen E, Buschard K, Hakomori S, Young WW (1984) Pattern of distribution of blood group antigen on human epidermal cells during maturation. J Invest Dermatol 82:13–17

    Google Scholar 

  • Dechesne CJ, Pujol R (1986) Neuron-specific enolase immunoreactivity in the developing mouse cochlea. Hear Res 21:87–90

    Google Scholar 

  • Dechesne CJ, Sans A, Keller A (1985) Onset and development of neuron-specific enolase immunoreactivity in the peripheral vestibular system of the mouse. Neurosci Lett 61:299–304

    Google Scholar 

  • Dechesne CJ, Escudero P, Lamande N, Thomasset M, Sans A (1987) Immunohistochemical identification of neuron-specific enolase and calbindin in the vestibular receptors of human fetuses. Acta Otolaryngol [Suppl] (Stockh) 436:69–75

    Google Scholar 

  • DeGrauw T, Liwnicz B (1986) Lectins are markers of neuronal migration and differentiation in rat brain. Dev Neurosci 8:236–242

    Google Scholar 

  • Desmadryl G, Raymond J, Sans A (1985) Histogenesis of the vestibular sensory epithelium in organotypic culture of mouse embryo otocysts: a tritiated thymidine autoradiographic study. Int J Dev Neurosci 3:549–557

    Google Scholar 

  • Dodd J, Jessell TM (1985) Lactoseries carbohydrates specify subsets of dorsal root ganglion neurons projecting to the superficial dorsal horn of rat spinal cord. J Neurosci 5:3278–3294

    Google Scholar 

  • Edelman GM (1983) Cell adhesion molecules. Science 219:450–457

    Google Scholar 

  • Edelman GM (1984) Cell adhesion and morphogenesis: the regulator hypothesis. Proc Natl Acad Sci USA 81:1460–1464

    Google Scholar 

  • Edelman GM, Gallin WJ, Delouvee A, Cunningham BA, Thiery JP (1983) Early epochal maps of two different cell adhesion molecules. Proc Natl Acad Sci USA 80:4384–4388

    Google Scholar 

  • Feizi T (1985) Demonstration by monoclonal antibodies that carbohydrate structures of glycoproteins and glycolipids are oncodevelopmental antigens. Nature 314:53–57

    Google Scholar 

  • Feizi T, Childs RA (1987) Carbohydrates as antigenic determinants of glycoproteins. Biochem J 245:1–11

    Google Scholar 

  • Friedmann I (1969) The innervation of the developing fowl embryo otocyst in vivo and in vitro. Acta Otolaryngol (Stockh) 67:224–238

    Google Scholar 

  • Friedmann I, Bird ES (1967) Electron microscopic studies of the isolated fowl embryo otocyst in tissue culture, rudimentary kinocilia, cup-shaped nerve endings and synaptic bars. J Ultrastruct Res 20:356–365

    Google Scholar 

  • Friedmann I, Hodges MG, Riddle PN (1977) Organ culture of the mammalian and avian embryo otocyst. Ann Otol Rhinol Laryng 86:371–380

    Google Scholar 

  • Gane P, Vellayoudom J, Mollicone R, Breimer ME, Samuelsson BE, Rouger P, Gérard G, Le Pendu J, Oriol R (1987) Heterogeneity of anti-A and anti-B monoclonal reagents. Vox Sang 53:117–125

    Google Scholar 

  • Gil-Loyzaga P, Pujol R (1987) Trophic interactions between spiral ganglion neurons and the cochlear epithelium during in vitro development. 10th ARO Research Meeting, Clearwater Beach, Fla, p 223

  • Gil-Loyzaga P, Pujol R, Mollicone R, Dalix AM, Oriol R (1989) Appearance of B and H blood group antigens in the developing cochlear hair cells. Cell Tissue Res 257:17–21

    Google Scholar 

  • Ginzberg RD, Gilula N (1979) Modulation of cell junctions during differentiation of the chick otocyst sensory epithelium. Dev Biol 68:110–129

    Google Scholar 

  • Ginzberg RD, Gilula N (1980) Synaptogenesis in the vestibular sensory epithelium of the chick embryo. J Neurocytol 9:405–424

    Google Scholar 

  • Hakomori S (1981) Blood group A, B, H and ii antigens of human erythrocytes: chemistry, polymorphism, and their development changes. Semin Hematol 18:39–62

    Google Scholar 

  • Jacobson M (1978) Cellular interactions and interdependence during development of the nervous system. In: Jacobson M (ed) Developmental neurobiology, 2nd. Plenum, New York London, pp 253–307

    Google Scholar 

  • Knowlton VY (1967) Correlation of the development of membranous and bony labyrinths, acoustic ganglia, nerves, and brain centers of the chick embryo. J Morphol 121:179–208

    Google Scholar 

  • Legrand C, Bréhier A, Clavel MC, Thomasset M, Rabié A (1988) Cholecalcin (28-kDa CaBP) in the rat cochlea. Development in normal and hypothyroid animals. An immunocatochemical study. Dev Brain Res 38:121–129

    Google Scholar 

  • Le Pendu J (1989) A hypothesis on the dual significance of ABH, Lewis and related antigens. J Immunogenet 16:53–61

    Google Scholar 

  • Le Pendu J, Lemieux RU, Lambert F, Dalix AM, Oriol R (1982) Distribution of H type 1 and H type 2 antigenic determinants in human sera and saliva. Am J Human Genet 34:402–415

    Google Scholar 

  • Le Pendu J, Lemieux RU, Dalix AM, Lambert F, Oriol R (1983) Competition between ABO and Le gene specified enzymes. Vox Sang 45:349–358

    Google Scholar 

  • Le Pendu J, Dalix AM, Mollicone R, Crainic K, Oriol R (1989) Expression of ABH, Lewis and related tissue antigens in the human thymus. J Immunogenet 16:19–32

    Google Scholar 

  • Mackenzie IC, Dabelsteen E (1987) Connective tissue influences on the expression of epithelial cell-surface antigens. Cell Tissue Res 248:137–141

    Google Scholar 

  • Mbienne JP, Favre D, Sans A (1988) Early innervation and differentiation of hair cells in the vestibular epithelia of mouse embryos: SEM and TEM study. Anat Embryol 177:331–340

    Google Scholar 

  • Mbienne JP, Dechesne CJ, Schachner M, Sans A (1989) Immunocytochemical characterization of the expression of cell adhesion molecule L1 during early innervation of mouse otocysts. Cell Tissue Res 255:81–88

    Google Scholar 

  • Mollicone R, Bara J, Le Pendu J, Oriol R (1985a) Immunohistologic pattern of type 1 (Lea, Leb) and type 2 (X, Y, Z) blood group related antigens in the human pyloric and duodenal mucosae. Lab Invest 53:219–227

    Google Scholar 

  • Mollicone R, Trojan J, Oriol R (1985 b) Appearance of H and B antigens in primary sensory cells of the rat olfactory apparatus and inner ear. Dev Brain Res 17:275–279

    Google Scholar 

  • Mollicone R, Davies DR, Evans B, Dalix AM, Oriol R (1986) Cellular expression and genetic control of ABH antigens in primary sensory neurons of marmoset, baboon and man. J Neuroimmunol 10:255–269

    Google Scholar 

  • Oriol R (1990) Genetic control of the fucosylation of ABH precursor chains. Evidence for new epistatic interactions in different cells and tissues. J Immunogenet 17:235–245

    Google Scholar 

  • Oriol R, Mancilla-Jiménez R (1983) Fluorescent staining nuclei and amyloid substance. Two useful properties of p-phenylene-diamine. J Immunol Methods 62:185–192

    Google Scholar 

  • Oriol R, Cooper JE, Davies DR, Keeling PWN (1984) ABH antigens in vascular endothelium and some epithelial in baboons. Lab Invest 50:514–518

    Google Scholar 

  • Oriol R, Le Pendu J, Mollicone R (1986) Genetics of ABO, Lewis, X and related anigens. Vox Sang 51:161–171

    Google Scholar 

  • Oriol R, Samuelsson BE, Messeter L (1990) ABH antibodies-serological behaviour and immunochemical characterization. J Immunogenet 17:279–299

    Google Scholar 

  • Orr MF (1968) Histogenesis of sensory epithelium in reaggregates of dissociated embryonic chick otocysts. Dev Biol 17:39–54

    PubMed  Google Scholar 

  • Pfenninger KH, Maylie-Pfenninger MF, Friedmann LB, Simkowitz P (1984) Lectin labelling sprouting neurons III: type specific glycoconjugates on growth cones of different origin. Dev Biol 106:97–108

    PubMed  Google Scholar 

  • Pujol R, Lavigne-Rebillard M (1985) Early stages of innervation and sensory cell differentiation in the human fetal organ of Corti. Acta Otolaryngol (Stockh) [Suppl] 423:43–50

    Google Scholar 

  • Pujol R, Sans A (1986) Synaptogenesis in the cochlear and vestibular receptors. In: Aslin R (ed) Advances in neural and behavioural development, vol. 2. Ablex Press, Norwood, New Jersey, pp 1–18

    Google Scholar 

  • Raymond J (1987) In vitro differentiation of mouse embryo statoacoustic ganglion and sensory epithelium. Hear Res 28:45–56

    Google Scholar 

  • Reibel J, Dabelsteen E, Hakomori S, Young WW, Mackenzie IC (1984) The distribution of blood group antigens in rodent epithelia. Cell Tissue Res 237:111–116

    Google Scholar 

  • Rose JE, Sobkowicz HM, Bereman B (1977) Growth in culture of the peripheral axons of the spiral neurons in response to the displacement of the receptors. J Neurocytol 6:49–70

    Google Scholar 

  • Roth J, Taatjes DJ, Bitter-Suermann D, Finne J (1987) Polysialic acid units are spatially and temporally expressed in developing postnatal rat kidney. Proc Natl Acad Sci USA 84:1969–1973

    Google Scholar 

  • Rutishauser U (1984) Developmental biology of a cell adhesion molecule. Nature 310:594–597

    Google Scholar 

  • Sher AE (1971) The embryonic and postnatal development of the inner ear of the mouse. Acta Otolaryngol [Suppl] (Stockh) 285:1–77

    Google Scholar 

  • Smits-Van Prooije AE, Poelmann RE, Gesink AF, Groeningen MJ van, Vermeij-Keers CHR (1986) The cell surface coat in neurulating mouse ant rat embryos, studied with lectins. Anat Embryol 175:111–117

    Google Scholar 

  • Steindler DA, Cooper NGF (1987) Glial and glycoconjugate boundaries during postnatal development of the central nervous system. Dev Brain Res 36:27–38

    Google Scholar 

  • Steward O (1989) The formation of neural connections. II: Dendritic development and the establishment of synaptic connections. In: Steward O (ed) Principles of cellular, molecular and developmental neuroscience. Springer, Berlin Heidelberg New York, pp 181–217

    Google Scholar 

  • Tello JF (1931) Le réticule des cellules ciliées du labyrinthe chez la souris et son indépendance des terminaisons nerveuses de la VIII paire. Trav Lab Recher Biol 27:151–186

    Google Scholar 

  • Thornhill RA (1972) The development of the labyrinth of the lamprey (Lampetra fluviatilis). Proc R Soc Lond (Biol) 181:175–198

    Google Scholar 

  • Thorpe SJ, Bellairs R, Feizi T (1988) Developmental patterning of carbohydrate antigens during early embryogenesis of the chick: expression of antigens of the poly-N-acetyllactosamine series. Development 102:193–210

    Google Scholar 

  • Van de Water TR (1976) Effects of removal of the statoacoustic ganglion complex upon the growing otocyst. Ann Otol Rhinol Laryngol [Suppl] 85:1–32

    Google Scholar 

  • Van de Water TR (1986) Determinants of neuron-sensory receptor cell interaction during development of the inner ear. Hear Res 22:265–277

    Google Scholar 

  • Watkins WM (1980) Biochemistry and genetics of the ABO, Lewis and blood group systems. Adv Hum Genet 10:1–136

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departmento Ciencias Morfologicas, Facultad de Medicina, Universidad Complutense, Apartado de Correos 60075, E-28080, Madrid, Spain

    Pablo Gil-Loyzaga & Manuel Remezal

  2. CNRS, Biochimie, Faculté de Pharmacie, Université Paris-Sud, Chatenay-Malabry, France

    Rafael Oriol

Authors
  1. Pablo Gil-Loyzaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manuel Remezal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rafael Oriol
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gil-Loyzaga, P., Remezal, M. & Oriol, R. Neuronal influence on B and H human blood-group antigen expression in rat cochlear cultures. Cell Tissue Res 269, 13–20 (1992). https://doi.org/10.1007/BF00384721

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00384721

Key words

Search

Navigation