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Title: The Expressions of Luteinizing Hormon and Sex Steroid Receptors in Human Fallopian Tube During the Menstruel Cycle

Authors:
1.Ecmel ISIK KAYGUSUZ, Pathology, Zeynep Kamil Maternity and Pediatric Research and Training Hospital, Istanbul, Turkey, 34668,  HYPERLINK "mailto:ecmeli@yahoo.com" ecmeli@yahoo.com. Burhanettin Ust�nel cad. No:10, Uskudar, Istanbul. (corresponding author)
2.Hulya YAVUZ, Pathology, Zeynep Kamil Maternity and Pediatric Research and Training Hospital, Istanbul, Turkey, 34668. Burhanettin Ust�nel cad. No:10, Uskudar, Istanbul.
3.Handan CET0NER, Pathology, Zeynep Kamil Maternity and Pediatric Research and Training Hospital, Istanbul, Turkey, 34668. Burhanettin Ust�nel cad. No:10, Uskudar, Istanbul.
4.Suna CESUR, Pathology, Zeynep Kamil Maternity and Pediatric Research and Training Hospital, Istanbul, Turkey, 34668. Burhanettin Ust�nel cad. No:10, Uskudar, Istanbul.
5.Ceylan YOZGATLIGIL, Department of Statistics, METU, Ankara, 06800. Universiteler Mah. Dumlup1nar Bulvar1, No:1, Cankaya, Ankara
6.Selcuk AYAS, Department of Obstetric and Gynecology, Zeynep Kamil Maternity and Pediatric Research and Training Hospital, Istanbul, Turkey, 34668. Burhanettin Ust�nel cad. No:10, Uskudar, Istanbul.







												


ABSTRACT

Objective: Expression  of  receptors  for  LH  has  been  demonstrated  in  the  human  Fallopian  tube;  however  their  role  in  the  physiology of the Fallopian  tube  is  still  unknown. During  the  normal  menstruel  cycle,  the  female  reproductive  system  is  exposed  to  fluctuating  levels  of  sex  steroids,  including  estrogen   and  progesterone.  In  this  study,  we present the  cyclical  variations  of  tubal  LH,  ER,  PR  receptors.
Materials and Methods:Twenty healthy women operated for benign causes were included in the study. Fallopian tubes from the different stages of the menstruel cycle were collected and examined using immunohistochemistry.
Results: Expression  of  LH  receptor  did  not  change  according  to  phases  of menstrual  cycle and there  is  no  significant  difference  between  follicular  phase  and  luteal  phase  groups. According  to  the  result  of  statistically analized,  there  is  not  a  significant  difference  between  the  PR  of  follicular  phase  and  luteal  phase.
Conclusion: We  report  on  differences  in  LHR,  SHR  expression  in  Fallopian  tube  from  women  with  follicular  phase  compared  with  luteal  phase. These data are an important benchmark for furthering the understanding of normal human Fallopian tubes physiology.


Key Words: Luteinizing Hormon, Fallopian tube, immunohistochemistry.





INTRODUCTION
LH  (Luteinizing  Hormon)  and  it�s  agonist,  hCG,  play  a  important  role  in  the  regulation  of  gonadal  physiology  (1).  LH  and  hCG  are structural  and  functional  homologs  that  bind  to  the  same  receptors   (2).  The  receptors  are  transmembrane  glycoproteins  that  belong  to  the  G  protein-coupled  receptor  superfamily  (3,4).  They  consist   of  equal  size  exo-  and  endo-domains.  The  exodomain contains  hormone  binding  sites  and  endodomain  contains  seven transmembrane  regions  and  a  short  cytoplasmic  tail  that  is  coupled  to  signal  transduction  pathways  (3,4). Expression  of  receptors  for  LH  has  been  demonstrated  in  the  human  Fallopian  tube  (5);  however  their  role  in  the  physiology of the Fallopian  tube  is  still  unknown.
Studies  have  shown  that  a  number  of  nongonadal  tissues,  including  human  uterus,  tuba  uterina,  also  contain  LH  receptors (LHR)  (5,6,7,8)  and  the  tubal  receptors  are  present  mainly  in mucosal  cells,  but  also  in  the  smooth  muscle  and  blood vessels  endothelium  (5).
The  results  of  the  animal  studies  suggested  that  estradiol promotes  LHR  synthesis  in  the  epithelium  and  smooth  muscle and, along  with  LH,  causes  the  relaxation  of  the  porcine  oviduct, especially  during  the  periovulatory  stage  of  the  estrious  cyle (1,9,10,11).  The  results  of  the  animal  study  indicated  that  LH  can  control oviductal  contractions  directly  and  may  be  partially  responsible  for  the  relaxation  of  istmus  during  fertilization  in  pigs (1). 
During  the  normal  menstruel  cycle,  the  female  reproductive  system  is  exposed  to  fluctuating  levels  of  sex  steroids,  including  estrogen   and  progesterone.  A  number  of  studies  have  investigated  the  expression  patterns  of  estrogen  (ER),  progesterone  (PR)  receptors in  the  human  endometrium.  However,  the  expression  of  sex  steroid hormone  receptors  (SHR)  has  yet  to  be  comprehensively  studied  in  the  normal  human  Fallopian  tube.  SHR  belong  to  a  superfamily  of  genes  that  function  as  ligand-activated  transcription  factors  (12).
ER  was  immunolocalized  to  epithelial  cells  in  the  ampullary  and  fimbrial  sections  of  the  Fallopian  tube  and  was  reputed  to  increase throughout  the  follicular  phase  before  reaching  a  plateau  in  the  luteal  phase  (13).  Expression  of  PR  in  the  Fallopian  tube  was  first  characterized  in the  early  1990�s  (13,14).  These  studies  showed  that  immuno expression  of  epithelial  PR  expression  was  most  intense  in  the follicular  phase  but  that  it  was  not  detected  in  the  late  luteal  phase  (13).
Sex  steroid-regulated  changes  in  Fallopian  tube  gene  expression and  function  likely  contribute  to  successful  embryo  tubal  transport  and  implantation.  Detailed  knowledge  of  LHR  and  SHR  expression  patterns  in  human  Fallopian  tube  during  the  menstruel cycle  and  is  therefore  important  for  furthering  the  understanding  of Fallopian  tube  biology.
In  this  study,  the  cyclical  variations  of  tubal  LH,  ER,  PR  receptors are  reported  and  compared.

MATERIAL-METHODS
Twenty  Fallopian  tubes  were  collected  at  the  different  phases  of  the  menstrual  cycle  from  twenty  women  who  were  undergoing  routine  total  abdominal  hysterectomy  (TAH)  for  benign  disease  not  affecting  the  Fallopian  tubes. All  women  had  regular  menstrual  cycles,  were  of  proven  fertility  with  no  evidence  of  tubal  disease  and  were  not  taking  exogenous  hormanes. Totally  twenty  Fallopian  tubes  were  collected,  ten  of  these  cases  are  in  the  follicular  phases  (median  age  45 years,  range  42-49  years)  and  ten  of  these  cases  are  in  the  luteal  phases (median  age  45  years,  range  41-48  years)  of  the  menstrual  cycle.

Histological  dating  was  carried  out  according  to the  criteria  of  Noyes  et  al.  (1975)  to  confirm  the  phase  of  the  menstryal  cycle  and  all endometrial  samples  from  the  different  phases  of  the  cycle  were  consistent  for  the  patient�s reported  last  menstrual period  (LMP),  steroid  hormones  concentrations  and   histological  stage  (Table I).
Sampling
For  the  case  group,  the  Fallopian  tubes  were  excised  and  to  assure  the  integrity  of  tubal  morphology  and  function.  The  Fallopian  tubes  were  fixed  in  10%  formalin,  sectioned   serially,  embedded  in  paraffin  blocks  and  underwent  hematoxylin- eosin  staining  for  light  microscopic  analysis.
Immunohistochemistry
An  avidin-biotin  horseradish  peroxidase  tecnique  was  used  to  localize  the expression  of  LH,  ER,  PR  in  the  different  samples  using  LH/hCG receptor,  ER  receptor  (SP1),  PR  receptor  (SP2)  antibodies.  Briefly,  sections  were  dewaxed,  dehydrated  in  alcohol  and  treated  with  2%(vol/vol)  hydrogen peroxidase  for  20  min  in  methanol  to  block  endogenous  peroxidase.  The  sections  used  were  pre-trated  in  an  850-watt  domestic  microwave  oven  in  0.01  M  citrate  buffer  for  5  min.  The  sections  were  incubated  for  30  min  with  normal  horse  serum  (Vector  Laboratories,  Burlingham,  CA,  USA)  and  then  incubated  with  the  primary  antibodies  overnight  at  4  C.  The  antibody  concentrations  were  1:1000  and  1:20  for  BC2  and  214D4,  respectively.  The  following  day  the  sections  were  washed  with  20mM  phpspate  buffered  saline  (pH 7.3)  and  then  incubated  with  1:200  biotinylated  horse  anti-mouse  secondary  antibody  for  30  min.  After  a  further  wash  step,  the  sections  were  incubated  with  the  avidin-biotin  peroxidase  complex  ELITE  system  (Vector Laboratories,  Inc.,  Burlingham,  CA,  USA)  for  30  min  and  then  subsequently with  3,3�-diaminobenzidine  (Vector  Laboratories,  Burlingham,  CA,  USA)  for  10  min.  Sections  were  washed  in  tap  water,  counter  stained  with  Gill�s haematoxylin,  then  dehydrated  in  a  series  of  graded  ethanol,  cleared  in  xylene  and  mounted  in  DPX  (Biostain,  Manchester,  UK). 
Estrogen  and  progesterone  receptor  immunopositivity  were  semi-  quantitatively  evaluated.   Reactions  were  interpreted  is  positive  based  on  nuclear  staining  for  ER,  PR  receptor�s  and  as  positive  based  on  cytoplasmic  staining  for  LH   receptors.  Immunohistochemical  staining  results  for  ER,  PR  receptors were  scored  based  on  the  percentage  of  cells  showing  expression.  The  scoring  system  was:  0=<5%;  +1=6-25%;  +2=26-50%;  +3=51-75%;  +4=76-100%. 
Statistical  Analysis
Existence  of  possible  differences  among   follicular  phase  groups  and  luteal  phase  groups  was  analyzed  by  Kruskal-Wallis  test  due  to having  sample  sizes  less  than  30.  Having  significant  results  leaded  the  post-hoc  analysis.  Pairwise  comparisons  were  performed  by  Mann-Whitney-U  test. SPSS  17  for  Windows  (SPSS,  Inc.,  Chicago,  IL)  was  used.  P-values  <  0.05  were  regarded  as  significant.  For  the  post-hoc  analysis,  Bonferroni  adjustment  was  used.

RESULTS

LH immunohistochemistry
  Follicular  Phase:  LH  receptor  was  immunolocalized  in  the  apical  localization  in  the  epithelial  cells.  Only  two  samples  had  the  muscle  cells  of  myosalpix  contained  receptors (Figure 1, 2).  The  receptor  immunostaining  was  not  detected  in  the  tubal  blood  vessels  endothelium.
  Luteal  Phase:  Immunohistochemistry  demonstrated  the  presence  of  receptor  immunostaining  in  the  tubal  mucosa  and  smooth  muscle  cells (Figure 3,4).  All  samples  had  showed  the  presence  of  LH  receptors  in  the  tubal  mucosa,  but  only  two  samples  had  the  muscle  cells  of  myosalpinx  contained.
The  frequency  of  the  existence  of  LH  receptors  on  tubal  mucosal epithelium,  muscle  cells  and  blood  vessel  endothelium  for  menstrual  cycle  group  have  showed  Table  II.
LH  receptor  seen  on  muscle  is  lower  for  follicular  phase  and  luteal  phase  groups  (2/18).  Expression  of  LH  receptor  did  not  change  according  to  phases  of menstrual  cycle.


ER immunohistochemistry
  Follicular  Phase:  Positive  staining  was  observed  in  eight  tissue  samples  for the  ER  receptors.  Immunoreactivity  for  ER  receptor  in  the  Fallopian  tube sections  was  seen  in  the  epithelium  of  the  mucosa  and  endosalpingeal  stromal  cells (Figure 5).  The  mean  value  of  staining  intensity  for   ER  receptor  was  moderate  (Score:+2) (Table  III).
  Luteal  Phase:  Positive  staining  was  observed  in  seven  tissue  samples  for  the ER  receptors.  Immunoreactivity  for  ER  receptor  in  the  Fallopian  tube  sections was  seen  in  the  epithelium  of  the  tubal  mucosa  and  endosalpingeal  stromal cells.  The  mean  value  of  staining  intensity  for  ER  was  moderate (Score:+2)  (Table  III).
There  is  no  significant  difference  between  follicular  phase  and  luteal  phase  groups  (p-value=0.631). 

PR immunohistochemistry
Follicular Phase:  PG  receptors  demostrated  immunoreactivity  during   all  cases.  The  antibody  clearly  stained  epithelium  of  the  tubal  mucosa  and  endosalpigeal  stromal  cells (Figure 6)  and  the staining  scores  was  moderate   in  follicular  phase  (Score:+2).

Luteal Phase:  PG  receptors  demostrated  immunoreactivity  during  all  menstrual  cycle  phases  and  all  cases.  The  antibody  clearly  stained  epithelium  of  the  tubal  mucosa  and  endosalpigeal  stromal  cells  and  the  staining  scores  were  very  strong  in  luteal  phase  (Score:+4).  PR  scores  were  generally  high  in  the  luteal  phase  than  the  follicular  phase.
According  to  the  result  of  Kruskal-Wallis,  there  is  not  a  significant  difference  between  the  PR  of  follicular  phase  and  luteal  phase.

DISCUSSION
In  this  study  the  cyclical  variations  of  the  Fallopian  tube  LH,  ER  and  PR  receptors  are  compared.
The  major  function  of  the  Fallopian  tube  is  the  transport  of  gametes  to  the  ampullary-isthmic  junction,  the  usual  site  of  fertilization  and  transport  of  embryos  to  the  uterus. In  the  in  vitro  animal  studies  of  Fallopian  tube  contractility,  the  greatest  effect  of  LH  on  relaxation  of  Fallopian  tube  occurred  during  the  peri-ovulatory  stage  of  the  menstrual  cycle  and  the  results  of  this  investigation  indicate  that  LH  should  be  added  to  the  list  of  factors  affecting  Fallopian  tube  function  (1,15).  LH  plays  an  important  role  in  controlling  Fallopian  tube  contractions,  and  is  a  major  factor  responsible  for  opening  the  ampulla-istmic  junction  for  spermatozoa  and  for  synchronization  of  fertilization  of  ova  in  the  ampulla.  In  this  study,  we  performed  immunohistochemistry  to  detect  the  presence  or  absence  of  LH  receptor  expression  in  women  with  normal  menstrual  cycle  Fallopian  tubes,  and  statistical  analysis  was  performed  to  see  the  difference  between  menstrual  cycle  groups  (follicular  phase  and  luteal  phase).  We  have  not  shown  a  quiet  difference  in  LH  receptor  expression  in  Fallopian  tube  from  women  with  follicular  phase  compared  with  luteal  phase.  LH  receptor  was  immunolocalized  in  the  apical  cells in all cases.  In  the  follucular  phase  only  two  samples  had  the  muscle  cells  of  myosalpinx  contained  receptors.  The  receptor  immunostaining  was  not  detected  in  the  tubal  blood  vessels  endothelium.
In  the  luteal  phase,  immunohistochemistry  demonstrated  the  presence  of  receptor  immunostaining  in  the  tubal  mucosa  and  smooth  muscle  cells.  All  samples  had  showed  the  presence  of  LH receptors  in  the  tubal  mucosa,  but  only  two  samples  had  the  muscle  cells  of  myosalpinx  contained.
The  female  reprodictive  system  is  exposed  to  fluctuating  levels  of  sex  steroids,  including  estrogen  and  progesterone,  during  the  normal  menstrual  cycle.  However,  the expresiion  of  sex  steroid  hormone  recptors  has  yet  to  be  comprehensively  studied  in  the  normal  human  Fallopian  tube  or  in  the  context  of  tubal  pathologies.
Tubal  ER  receptors  are  maximal  at  midcycs,  whereas  progesterone  receptors  are  present  throughout  the  cycle;  even  into  the  late  luteal  phase  (13).  Two  ER  genes  have  been  identified:  ER  alpha  and  ER  beta.  Expression  of  ER  alpha  or  ER  beta  has  not  been  examined  in  the  Fallopian  tube  from  women with  ectopic  pregnancy.  Estrogen  stimulates  epithelial  cell  hypertrophy,  secretion  and  ciliogenesis,  whilst  atrophy  and  decilination  are  associated  with  high  levels  of  serum  progesterone  (16).  
Progesterone  receptors  are  present  throughout  the  cycle,  even  into  the  late  luteal  phase.  Progesterone  has  been  suggested  to  have  an  inhibitory  action  on  tubal  activity,  as  high  progesterone  levels  in  the  luteal  phase  coincides  with  reduced  fruquency  of  contractions  (17,18,19).  This  inhibitory  effect  of  progesterone  might  be  of  importance  in  relaxation  of  the  physiological  sphincter  in  the  isthmus,  allowing  cilia  to  transport  the  pre-embryo  in  to  the  uterine  cavity  (20). 
In  this  study,  we  also  performed  immunohistochemistry  to  detect  the  presence  and  intensity  of  SHR  expression  in  women  with  normal  menstrual  cycle  Fallopian  tubes,  and  statistical  analysis  was  performed  to  see  the  difference  between  menstrual  cycle  groups (follicular  phase  and  luteal  phase).
In  the  follicular  phase,  positive  staining  was  observed  in  eight  tissue  samples  for  the  ER  receptors.  Immunoreactivity  for  ER  receptor  in  the  Fallopian  tube  sections  was  seen  in  the  epithelium  of  the  mucosa  and  endosalpingeal  stromal  cells.  The  mean  value  of  staining  intensity  for   ER  receptor  was  moderate  (Score:+2) (Table  III).
In  the  luteal  phase,  positive  staining  was  observed  in  seven  tissue  samples  for  the  ER  receptors.  Immunoreactivity  for  ER  receptor  in  the  Fallopian  tube  sections  was  seen  in  the  epithelium  of  the  tubal  mucosa  and  endosalpingeal  stromal  cells.  The  mean  value  of  staining  intensity  for  ER  was  moderate  (Score:+2)  (Table  III).
Our  study  has  shown  that  there  is  not  a  significant  difference  between  the  ER%  of  follicular  phase  and  luteal  phase. 
PG  receptors  demostrated  immunoreactivity  during  all  groups  and  cases.  The   antibody  clearly  stained  epithelium  of  the  tubal  mucosa  and  endosalpigeal  stromal  cells  and  the  staining  scores  were  very  strong  in  luteal  phase  group  (Score:+4)  comparing  follicular  phase  group  (Score:+2).  According  to  our  result,  there  is  a  a  significant  difference  between  the  PR%  of  follicular  phase  group  and  luteal  phase  group.  PR  scores  were  generally  high  in  the  luteal  phase  than  the  follicular  phase.  Progesterone  might  have  a  physiological  function  by  regulating  relaxation  of  the  istmic  sphincter.  And  progesterone  seem  to  have  a  role  to  play  in  the  transport  of  gametes  and  pre-embryos  in  the  Fallopian  tube.
In  the  summary,  we  report  on  differences  in  LHR,  SHR  expression  in  Fallopian  tube  from  women  with  follicular  phase  compared  with  luteal  phase.  These  findings  may  suggest  that  to  play  an  important  role  in  influencing  tubal  functions  and  embryo  transport  to  the  uterus.









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