Ultrastructural features of the Fallopian tube epithelium ...

The Journal of Basic & Applied Zoology (2013) 66, 148–153

The Egyptian German Society for Zoology

The Journal of Basic & Applied Zoology

www.egsz.orgwww.sciencedirect.com

Ultrastructural features of the Fallopian tube epithelium

of bat, Taphozous longimanus (Hardwicke)

A.A. Nerkar *,1, M.M. Gadegone2

Reproductive Biology Section, Department of Zoology, Institute of Science, Nagpur University, Nagpur 440001 (MS), India

Received 15 February 2013; revised 4 July 2013; accepted 31 July 2013Available online 24 August 2013

*

71

E

Pe

Z

20

ht

KEYWORDS

Bat;

Ultrastructure;

Fallopian tube;

Tubal epithelium;

Ampulla;

Isthmus

Corresponding author. T

225265581.

-mail address: archana_nerk1 Associate Professor2 Professor

er review under responsibilit

oology.

Production an

90-9896 ª 2013 Production

tp://dx.doi.org/10.1016/j.joba

el.: +

ar1@yah

y of The

d hosti

and host

z.2013.07

Abstract The epithelium of the Fallopian tube of Taphozous longimanus consists of two types of cells,

ciliated and nonciliated secretory cells. The ciliated cells of tubal epithelium possess motile cilia (kino-

cilia) that emerge through the luminal membrane. The cytoplasm of the ciliated cells contains large lipid

complex, abundance of polyribosomes, well developed Golgi apparatus, tubular ER and large number

ofmitochondria. The presence of fibrous granules, basal bodies, and ciliary buds indicates the process of

ciliogenesis in the Fallopian tube. The nonciliated secretory cells of ampulla show balloon-like bulges

which contain secretory granules. These cells were characterized by well developed rough endoplasmic

reticulum, numerous polyribosomes and secretory granules of varied size, shape, and density. The secre-

tory blebs were seen releasing into the lumen containing cell organelles. However, in some secretory

blebs nucleus along with cell organelles were observed. The nonciliated secretory cells of isthmus show

blunt cytoplasmic projection. Organelles such as mitochondria, Golgi apparatus, endoplasmic reticu-

lum and secretory granules were seen in the cytoplasm. The presence of numerous mitochondria, a well

developedGolgi apparatus and rough endoplasmic reticulum in both the ampulla and the isthmus indi-

cates that tubal epithelium was responsible for the synthesis of protein secretion.ª 2013 Production and hosting by Elsevier B.V. on behalf of The Egyptian German Society for Zoology.

Introduction

The oviductal epithelium consists of two morphological dis-tinct cell types, ciliated and nonciliated. The nonciliated cells

91 7122225311; fax: +91

oo.co.in (A.A. Nerkar).

Egyptian German Society for

ng by Elsevier

ing by Elsevier B.V. on behalf of T

.006

synthesize and release secretory materials (Bjorkman andFredricsson, 1960). Secretory products originating from the

oviductal epithelial cells have been identified and characterizedin several mammalian species (Abe, 1996). Some of these ovi-duct specific glycoproteins are associated with the zona pellu-

cida of ova and or the surface of the spermatozoa and mayplay important roles in fertilization, early development andfunctions of spermatozoa (Hunter, 1994; King et al., 1994;

Buhi et al., 2000; Abe et al., 1995b; Gandolfi, 1995; Killian,2004; Bhatt et al., 2004). Thus, it is tempting to speculate thatoviductal secretions create an important microenvironment for

fertilization and early embryonic development.Detailed electron microscopic studies on mammalian ovi-

ductal epithelial cells have been carried out by many workers(Bjorkman and Fredricsson, 1960; Nilsson and Reinius,

he Egyptian German Society for Zoology.

Figure 2 Electron micrograph of the ciliated cell showing a cross

section through a group of cilia with 9 + 2 arrangement and cross

section through a group of basal bodies (BB) with 9 peripheral

triplet fibrils and no central fibrils. Mitochondria (M) and Golgi

apparatus (G) are prominent. The cell surface has numerous

microvilli (Mv) (X 15,000).

igure 1 Electron micrograph of the ciliated epithelial cells

howing a broad apex and narrow base. The ciliated cells show a

rge number of rod shaped mitochondria (M), elongated cilia (Ci)

t apical end, indented nucleus (N) and lipid droplets (LD) at

franuclear cytoplasm. Basal cells are also seen (X 5000).

Ultrastructural features of the Fallopian tube epithelium of bat, Taphozous longimanus (Hardwicke) 149

1969; Odor et al., 1983; Abe and Oikawa, 1991; Abe, 1994;Abe et al., 1995). However, there is no report on the ultrastruc-tural characteristic of tubal epithelium of bat. A previous

study revealed that the oviductal epithelial cells of bat, Taph-ozous longimanus and Taphozous melanopogon secreted acidmucus glycoproteins (Sapkal and Gadegone, 1980; Gadegone

et al., 2002). In spite of the importance of these findings avail-able information on the secretory activity of epithelial cells ofthe bat oviduct is limited. The present study was undertaken to

examine the ultrastructural features of ciliated and nonciliatedsecretory cells in ampulla and isthmus regions of the Fallopiantube of the bat, T. longimanus (Hardwicke) during estrus toclarify the relationship between morphological features and

secretory activity.

Materials and methods

The emballonurid bat, T. longimanus (Hardwicke) was selectedfor the present study because of its unique reproductive habits.The specimens were collected from in and around Nagpur

(MS), India. The specimens were brought to the laboratoryalive. Mature females were separated from immature femalesafter observing mammary glands and pelvic dugs. Seven sexu-

ally mature female bats in estrus were killed by cervical dislo-cation for present investigation.

For the electron-microscopic study, transverse segments of

the ampullary and isthmic regions were obtained from theseFallopian tubes. Pieces of these segments were fixed in freshice-cold 3% glutaraldehyde for 3 h and then 4 h in 0.1 M cac-odylate buffer. The tissues were washed in buffer and then post

fixed for 1–2 h in 1% 0.067 M cacodylate-buffered osmiumtetroxide. After dehydration with graded series of alcohol,the tissues were cleared in propylene oxide solution and

embedded in Araldite resin which would be polymerized at60� C. Then, ultrathin sections from selected blocks were cutwith a glass knife and picked up on 400-mesh copper grids.

Sections were double stained with 10% alcoholic uranyl ace-tate for 20 min and for 10 min in Reynold’s lead citrate. Thesections were examined under a JEM Jeol-100s electron micro-

scope (Japan) at 80 KU accelerating voltage andphotographed.

Results

The Fallopian tube of T. longimanus shows some morpholog-ical differences. In the ampulla the muscular coat was thin andmucosa forms numerous elaborate branched folds. In the isth-

mus the muscular coat was thick and the longitudinal foldswere much shorter and less highly branched. The epitheliumof the Fallopian tube during estrus consists of ciliated and

nonciliated secretory columnar cells. These cells alternateirregularly in the epithelium. The apical portion of the noncil-iated secretory cells bulges over the ciliated cells and forms

protrusions or blebs which extend beyond the surface of themucous membrane.

The epithelium of the ampulla consists of ciliated and non-

ciliated secretory cells. The ciliated cells of ampullary regionwere columnar, broader at the luminal surface and narrow atthe base. They possess motile cilia (kinocilia) that emergethrough the luminal membrane. The ciliated cells have

interposed microvilli among the kinocilia (Fig. 1). Each cilium

F

s

la

a

in

is a slender, hair like process that extends from the free surface

of the cell. An extension of the cell membrane forms the ciliarymembrane. Within the ciliary membrane is the axoneme a bun-dle of 11 fibrils consisting of 2 central single fibrils and 9

peripheral double fibrils. One of the subfibrils of each periph-eral doublet has 2 short projections or arms. The fibrils wereembedded in a matrix material which appears to contain fibersradiating out to the peripheral fibrils like spokes in a wheel.

The basal bodies are lined up in orderly rows immediatelybeneath the cell membranes. Each basal body was a hollow,cylindrical structure. Embedded within the wall of the basal

body are 9 sets of triplet. Each triplet sets off an angle to theaxis of the basal body so that the cross sectional appearanceresembles a pinwheel. Fibrous rootlets with periodic cross-stri-

ation extend downward into the cytoplasm from the proximalend of each basal body (Fig. 2).

150 A.A. Nerkar, M.M. Gadegone

The ciliated cells contain a large lipid complex in the infra-nuclear part of the cytoplasm. The Golgi apparatus was welldeveloped and juxtanuclear in position. Polyribosomes were

observed in the cytoplasm. The rough endoplasmic reticulumwas in the form of short tubular cisternae dotted with ribo-somes. Numerous rod or round shaped mitochondria were

seen in the apical cytoplasm. Golgi lamellae show a parallelarrangement forming a circular area enclosing small and largevesicles and coated vesicles. The nucleus was elongated and the

nuclear membrane is indented. The heterochromatin was madeup of few chromatin clumps distributed in nucleoplasm and athin rim of heterochromatin was seen adherent to the innersurface of the nuclear membrane. Nucleolus was not observed.

The epithelium of isthmus shows less ciliation as compared tothat of ampulla. The ciliated cells were irregularly distributedand observed in groups among the nonciliated cells. The ultra-

structural features of ciliated cells of the isthmus were more orless similar to those described for the ciliated cells of theampullary region (Fig. 3).

During estrus, the ampullary secretory cells had balloon-like processes at their apical surfaces. The nucleus varied inshape and the nuclear membrane was indented. The hetero-

chromatin clumps were seen in the nucleoplasm. The secretorycells were characterized by rough endoplasmic reticulum and awell developed Golgi apparatus. The Golgi apparatus wasmade up of dilated saccules associated with several small ves-

icles as well as coated vesicles. The rough endoplasmic reticu-lum consists of lamellar, tubular, short and elongated cisternaedotted with ribosomes. Polyribosomes were also noticed in the

cytoplasm. Mitochondria were round and rod shaped withlamellar cristae distributed in the apical cytoplasm. The apicalsurface of secretory cells of the ampullary region showed

numerous microvilli extending into the lumen and filamentousmaterials were associated with these microvilli. Secretory gran-ules were observed in the supranuclear cytoplasm mostly be-

low the apical plasma membrane. The secretory granulespossessed homogenous electron-dense matrices. Some secre-tory granules appeared to be released by exocytosis. Multive-sicular body containing 3–4 dense bodies was seen in the

Figure 3 High power electron micrograph of the ciliated cell

showing elongated cilia and ciliary rootlets in the cytoplasm.

Mitochondria (M) are round to rod shaped, indented nucleus (N)

with few chromatin clumps, basal bodies (BB), lysosome (Ly),

microvilli (Mv) and elongated microfilaments are seen (X 15,000).

apical cytoplasm. The secondary lysosomes were also observedin the cytoplasm. The interdigitations and junctional com-plexes were observed between the adjacent epithelial cells.

The lumen of tube contains cytoplasmic apical secretory blebscontaining cytoplasmic organelles and secretory granules.Sometimes the apical secretory blebs contain nucleus along

with other organelles and secretory granules (Figs. 4 and 5).The nonciliated secretory cells of isthmic region have blunt

processes at their apical surfaces. The secretory cells were

columnar showing a narrow base and the apical portion wasslightly bulged. The microvilli were observed on the apical sur-face of the secretory cells. The secretory cells contain extensiverough endoplasmic reticulum and well developed Golgi appa-

ratus. Large number of mitochondria with lamellar cristae wasseen in the cytoplasm of the cell. Some lysosome-like bodieswere also observed. Multivesicular body containing 3–4 dense

bodies was observed. Electron-dense granules were present inthe cytoplasm as well as below the apical plasma membrane(Figs. 6 and 7). The secretory blebs were seen into the lumen.

These oval secretory blebs contain electron-dense granules justbelow the membrane. These dense granules were seen releasinginto the lumen by exocytosis (Fig. 8).

Discussion

In Taphozous, the tubal epithelium during the estrous phase is

composed of columnar ciliated and nonciliated secretory cellsas in other mammals (Nilsson and Reinius, 1969). Both the celltypes, ciliated and nonciliated alternate irregularly in the am-pulla and the isthmus. The presence of cilia was demonstrated

throughout the tubal epithelium. The structure of cilia is sim-ilar to that observed in other mammalian species (Hagiwaraet al., 2008). The presence of fibrous granules, basal bodies

and ciliary buds at estrus indicates that ciliogenesis in the Fal-lopian tube is stimulated by levels of endogenous estrogen.Rootlets are observed during estrus and their fine structure

indicates that they might function as anchoring structures forthe motile cilia. Glycogen granules in the cytoplasm of ciliatedand nonciliated cells of oviductal epithelium of bat are

Figure 4 The nonciliated cells of ampulla during estrus phase

have mitochondria (M) with lamellar cristae, tubular short

cisternae of endoplasmic reticulum (RER), lysosome (Ly) and

electron-dense secretory granules (Gr) in apical cytoplasm. The

cytoplasmic blebs are seen in the lumen. The blebs are with or

without nucleus (N). These cytoplasmic blebs have all cytoplasmic

organelles and secretory granules (X 10,000).

Figure 5 Electron micrograph of the ampullary secretory cell

showing extensive elongated tubular endoplasmic reticulum

(RER), and mitochondria (M) with lamellar cristae (X 25,000).

Figure 6 Electron micrograph of ciliated and nonciliated

epithelial cells of isthmus showing elongated cilia (Ci) on the

surface of ciliated cells and nonciliated cells showing blunt apical

projections containing electron-dense secretory granules (Gr) near

the apical membrane (X 6000).

Figure 7 High power electron micrograph of nonciliated cell

showing apical projection with one or two electron-dense granules

(Gr). Golgi complexes (G) are seen in the cytoplasm. Golgi

lamellae arranged parallely along with small non coated and

coated vesicles. Multivesicular body (MV) is seen (X 20,000).

Figure 8 High power electron micrograph of apical bleb from

nonciliated cell into the lumen. Secretory bleb contains secretory

granules (Gr) just below the apical membrane. Short tubular

cisternae of rough endoplasmic reticulum (RER) are distributed in

the cytoplasm. Some secretory granules are seen releasing into the

lumen (arrows). Cell organelles are not prominent in the bleb (X

25,000).

Ultrastructural features of the Fallopian tube epithelium of bat, Taphozous longimanus (Hardwicke) 151

observed during estrus (Sapkal and Gadegone, 1980). The

presence of electron-dense glycogen particles within basalbodies functions as a source of energy, for ciliary movementand the cytoplasmic glycogen as nourishment for the ovum.

Similar observations are reported in sheep (Murray, 1995); bo-vine (Nayak and Ellington, 1977); women (Verhage et al.,1979); dogs (Verhage et al., 1973); mammals (Nayak and

Wu, 1975); ewe (Nayak et al., 1976); armadillo (Codon andCasanave, 2009) supporting the present observations.

The ultrastructural characteristics of ciliated cells of both

the ampulla and isthmus of bat, showed well developed roughendoplasmic reticulum, numerous ribosomes, Golgi apparatusand numerous mitochondria. Lipid droplets are observed inthe infranuclear cytoplasm. The apical surface of ciliary cells

showed microvilli along with cilia. These morphological fea-tures of ciliated cells are similar to those described for ciliatedcells of Fallopian tubes of other mammals (Nayak and Wu,

1975; Nilsson and Reinius, 1969).The nonciliated secretory cells of the ampulla and the isth-

mus of T. longimanus during estrus are characterized by the

presence of extensive rough endoplasmic reticulum, well devel-oped Golgi apparatus, mitochondria, ribosomes and lyso-somal bodies. Similar ultrastructural features of nonciliatedcells and their synthetic machinery are reported in many mam-

mals (Abe and Oikawa, 1991; Abe, 1999; Murray, 1995; Nayaket al., 1976; Nayak and Ellington, 1977; Hollis et al., 1984;Nilsson and Reinius, 1969).

The cytoplasmic blebs with secretion are produced fromnonciliated secretory cells of the Fallopian tube of T. longim-anus. The cytoplasmic blebs are pinched off from the secretory

cells. Extruded nuclei along into the other cytoplasmic organ-elles are seen lying free in the tubal lumen. Similar observa-tions are reported in the other species of bats, Myotis

lucifugus lucifugus (Reeder, 1939), Glosophaga soricina(Rasweiler, 1972b) and T. melanopogon (Gadegone et al.,2002) and nonchiropteran mammals (Nilsson and Reinius,1969) supporting the present observations.

152 A.A. Nerkar, M.M. Gadegone

The secretory granules of oviductal epithelial secretory cellshave been investigated by means of electron microscopy inmany mammalian species. These studies have demonstrated

that the secretory cells contain several types of granules.Two types of secretory granules are observed in the oviductalsecretory cells of rabbit (Jansen and Bajpai, 1982); cow

(Bjorkman and Fredricsson, 1961); sheep (Hollis et al.,1984); monkey (Odor et al., 1983) and human (Bjorkmanand Fredricsson, 1962). Three types of secretory granules are

reported in bovine (Shackelford et al., 1970) and horse (Desan-tis et al., 2011) and four types of secretory granules are re-ported in sheep oviduct (Willemse and Van Vorstenbosch,1975). However, in bat oviduct only one type of electron-dense

secretory granule is observed. These observations suggest thatthere are marked differences among species in the morpholog-ical features as well as types of secretory granules and also sug-

gest that mammalian oviductal secretory cells producedifferent types of secretions.

The mammalian oviduct is a steroid responsive tissue where

gamete transports, fertilization, and early embryonic cleavagetake place. Estrous phase, follicular phase, and estrogen E2 in-duced oviduct secretory glycoprotein have been described in

several mammalian species (Abe, 1996; Kapur and Johnson,1988; Murray, 1993, 1995; DeSouza and Murray, 1994;Boatman and Magnoni, 1995; King et al., 1994; Abe andOikawa, 1991; Hunter, 1994; Bhatt et al., 2004; Buhi et al.,

2000; Lee and Yeung, 2006) and are proposed to be importantmediators in providing a suitable environment for these phys-iological processes. Jansen and Bajpai (1982) and Jansen

(1995) demonstrated histochemically acid mucus glycoproteinsin the ampulla and isthmus of oviduct. They suggested that,mucus glycoproteins would exert their most important effects

on spermatozoa ascending the reproductive tract and thenon fertilized ova enroute to the uterus. In T. longimanus, theoviductal secretion in ampulla and isthmus showed a high

amount of acid mucopolysaccharides during estrus as demon-strated histochemically (Sapkal and Gadegone, 1980). It is sug-gested that the acid glycoproteins secreted by the ampulla andthe isthmus of bat Fallopian tube may be interacting with zona

pellucida, perivitelline space and vitelline or blastomere mem-brane of ovulated eggs and early embryo may have a role inpreimplantation events which would have far reaching implica-

tions in assisted reproductive technology and in the develop-ment of non-hormonal contraceptive vaccine (Gandolfi et al.,1989; Abe and Oikawa, 1991; Buhi et al., 2000; Bhatt et al.,

2004; Killian, 2004). The structural basis for the mechanismswhereby the ampulla and the isthmus of bat contributes tothe biochemical milieu of the Fallopian tube is now well doc-umented. However, there is a need for further investigation

of biosynthesis and molecular biological data to support thepresent observations.

Acknowledgements

The electron microscopy facilities provided by Dr. Arun Chi-tale, Department of Histopathology, Jaslok Hospital and Re-search Centre, Mumbai (MS), India are gratefullyacknowledged. Our thanks are due to Mr. Dilip Kanaskar

and Shivaji Bhosale for their excellent technical assistance.

References

Abe, H., 1994. Regional variations in the ultrastructural features of

secretory cells in the rat oviductal epithelium. Anat. Rec. 240, 77–

85.

Abe, H., 1996. The mammalian oviductal epithelium: regional varia-

tions in cytological and functional aspects of the oviductal

secretory cells. Histol. Histopathol. 11, 743–768.

Abe, H., Onodera, M., Sugawara, S., Satoh, T., Hoshi, H., et al.,

1999. Ultrastructural features. J. Anat. 195, 515–521.

Abe, H., Oikawa, T., 1991. Regional differences in the ultrastructural

features of secretory cells in the golden hamster (Mesocricetus

auratus) oviductal epithelium. J. Anat. 175, 147–158.

Abe, H., Sendai, Y., Satoh, T., Hoshi, H., 1995. Bovine oviduct-

specific glycoprotein is a potent factor for the maintenance of the

viability and motility of bovine spermatozoa in vitro. Mol. Reprod.

Dev. 42, 226–232.

Bhatt, P., Kadam, K., Saxena, A., Natraj, U., 2004. Fertilization,

embryonic development and oviductal environment: role of estro-

gen induced oviductal glycoprotein. Indian J. Exp. Biol. 42, 1043–

1055.

Bjorkman, N., Fredricsson, B., 1960. The ultrastructural organization

and the alkaline phosphatase activity of the epithelial surface of the

bovine Fallopian tube. Z. Zellforsch. Mikrosk. Anat. 51, 589–596.

Bjorkman, N., Fredricsson, B., 1961. The bovine oviduct epithelium

and its secretory process as studied with the electron microscope

and histochemical tests. Z. Zellforsch. 55, 500–513.

Bjorkman, N., Fredricsson, B., 1962. Ultrastructural features of the

human oviduct epithelium. Int. J. Fertil. 7, 259–266.

Boatman, D.E., Magnoni, G.E., 1995. Identification of a sperm

penetration factor in the oviduct of the golden hamster. Biol.

Reprod. 52, 199–207.

Buhi, W.C., Alvarez, I.M., Kouba, A.J., 2000. Secreted proteins of the

oviduct. Cells Tissues Organs 166, 165–179.

Codon, S.M., Casanave, E.B., 2009. Morphology and histological

annual changes of the oviduct of Chaetophractus villosus (Mam-

malia, Xenarthra, Dasypodidae). Int. J. Morphol. 27 (355), 360.

Desantis, S., Zizza, S., Accogli, G., Acone, F., Rossi, R., Resta, L.,

2011. Morphometric and ultrastructural features of the mare

oviduct epithelium during oestrus. Theriogenology 75, 671–678.

DeSouza, M.M., Murray, M.K., 1994. An estrogen-dependent secre-

tory protein, which shares identity with chitinases, is expressed in a

temporal and regional specific manner in the sheep oviduct at the

time of fertilization and embryo development. Endocrinol. 136,

2485–2496.

Gadegone, M.M., Bhandarkar, W.R., Bhute, K., Romould, E.R.,

Watkar, G.R., 2002. Mucins in the Fallopian tube of the two

species of Indian bats. Trends in Life Sci. 15 (109), 117.

Gandolfi, F., 1995. Functions of proteins secreted by oviduct epithelial

cells. Microsc. Res. Tech. 32, 1–12.

Gandolfi, F., Brevini, T.A.L., Richardson, L., Brown, C.R., Moor,

R.M., 1989. Characterization of proteins secreted by sheep oviduct

epithelial cells and their function in embryonic development.

Development 106, 303–312.

Hagiwara, H., Ohwada, N., Aoki, T., Suzuki, T., Takata, K., 2008.

The primary cilia of secretory cells in the human oviduct mucosa.

Med. Mol. Morphol. 41, 193–198.

Hollis, D.E., Frith, P.A., Vaughan, J.D., Chapman, R.E., Nancarrow,

C.D., 1984. Ultrastructural changes in the oviductal epithelium of

Merino ewes during the estrous cycle. Am. J. Anat. 171, 441–456.

Hunter, R.H., 1994. Modulation of gamete and embryonic microen-

vironments by oviduct glycoproteins. Mol. Reprod. Dev. 39, 176–

181.

Jansen, R.P., Bajpai, V.K., 1982. Oviduct acid mucus glycoproteins in

the estrous rabbit: ultrastructure and histochemistry. Biol. Reprod.

26, 155–168.

Ultrastructural features of the Fallopian tube epithelium of bat, Taphozous longimanus (Hardwicke) 153

Jansen, R.P., 1995. Ultrastructure and histochemistry of acid mucus

glycoproteins in the estrous mammal oviduct. Microsc. Res. Tech.

32, 24–49.

Kapur, R.P., Johnson, L.V., 1988. Ultrastructural evidence that

specialized regions of the murine oviduct contribute a glycoprotein

to the extracellular matrix of mouse oocytes. Anat. Rec. 221, 720–

729.

King, R.S., Anderson, S.H., Killian, G.J., 1994. Effect of bovine

oviductal estrous-associated protein on the ability of sperm to

capacitate and fertilize oocytes. J. Androl. 15, 468–478.

Killian, G.J., 2004. Evidence for the role of oviduct secretions in sperm

function, fertilization and embryo development. Anim. Reprod.

Sci. 83, 141–153.

Lee, K.F., Yeung, W.S., 2006. Gamete/embryo-oviduct interactions:

implications on in vitro culture. Hum. Fertil. (Camb.) 9, 137–143.

Murray, M.K., 1993. An estrogen-dependent glycoprotein is synthe-

sized and released from the oviduct in a temporal- and region-

specific manner during early pregnancy in the ewe. Biol. Reprod.

48, 446–453.

Murray, M.K., 1995. Epithelial lining of the sheep ampulla oviduct

undergoes pregnancy-associated morphological changes in secre-

tory status and cell height. Biol. Reprod. 53, 653–663.

Nayak, R.K., Wu, A.S., 1975. Ultrastructural demonstration of cilia

and ciliary rootlets in mammalian uterine tube epithelium in

different functional states. Am. J. Vet. Res. 36, 1623–1630.

Nayak, R.K., Albert, E.N., Kassira, W.N., 1976. Cyclic ultrastructural

changes in ewe uterine tube (oviduct) infundibular epithelium. Am.

J. Vet. Res. 37, 923–933.

Nayak, R.K., Ellington, E.F., 1977. Ultrastructural and ultracyto-

chemical cyclic changes in the bovine uterine tube (oviduct)

epithelium. Am. J. Vet. Res. 38, 157–168.

Nilsson, O., Reinius, S., 1969. Light and electron microscopic structure

of the oviduct. In: Hafez, E.S.E., Blandau, R.J. (Eds.), The

Mammalian Oviduct. University of Chicago Press, Chicago, pp.

65–78.

Odor, D.L., Gaddum-Rosse, P., Rumery, R.E., 1983. Secretory cells of

the oviduct of the pig-tailed monkey, Macaca nemestrina, during

the menstrual cycle and after estrogen treatment. Am. J. Anat. 166,

149–172.

Reeder, E.N., 1939. Cytology of the reproductive tract of the female

bat, Myotis lucifugus lucifugus. J. Morphol. 64, 431–453.

Rasweiler, J.J., 1972. Reproduction in the long tongued bat,Glossoph-

aga soricina. I. Preimplantation development and histology of the

oviduct. J. Reprod. Fertil. 31, 249–262.

Sapkal, V.M., Gadegone, M.M., 1980. Histochemical observations on

the female reproductive tract of bats III. Mucosubstances in the

Fallopian tube of three species of bats. Folia. Histochemica. 18,

215–224.

Shackelford Jr., S.B., Dickey, J.F., Leland, T.M., Hill Jr., J.R., 1970.

Electron microscopy of the bovine oviduct ampulla. J. Animal. Sci.

30, 322–328.

Verhage, H.G., Bariether, M.I., Jaffe, R.C., Akbar, M., 1979. Cyclic

changes in ciliation, secretion, and cell height of the oviduct

epithelium in women. Am. J. Anat. 156, 505–522.

Verhage, H.G., Abel Jr., J.H., Tietz Jr., W.J., Barrau, M.D., 1973.

Estrogen-induced differentiation of the oviductal epithelium in

prepubertal dogs. Biol. Reprod. 9, 475–488.

Willemse, A.H., Van Vorstenbosch, C.J.A.H.V., 1975. The secretory

activity of the epithelium of the ampulla tubae in cyclic ewes: an

electron microscopical study. Tijdschrift. Voor. Diergeneeskunde.

100, 95–105.