ABSTRACT
Progesterone is essential for endometrial receptivity and successful establishment of pregnancy. Either an insufficient progesterone concentration or an insufficient response to progesterone, therefore can lead to infertility and pregnancy loss. Assessment of the role that either progesterone insufficiency or inadequate progesterone response plays in human reproductive failure has been difficult to assess because serum progesterone concentrations fluctuate markedly, limiting the ability to characterize sufficiency of progesterone, and there are no highly reliable markers of endometrial function available. Recent evidence demonstrates exquisite sensitivity of normal endometrium to very low levels of progesterone stimulation, suggesting that progesterone insufficiency should not be a common cause of reproductive failure. Further evidence suggests that women with endometriosis, and possibly polycystic ovarian syndrome, have an altered progesterone response, which may explain some of the clinical features of these disorders and supports the hypothesis that progesterone resistance underlies some cases of human reproductive failure.
KEYWORDS
Luteal phase defect - progesterone resistance - endometrium - embryo implantation - endometriosis
REFERENCES
1
Gellersen B, Fernandes M S, Brosens J J.
Non-genomic progesterone actions in female reproduction.
Hum Reprod Update.
2009;
2
Klein M.
[Berthold's article: Transplantation of the testes (1849)].
Arch Anat Histol Embryol.
1968;
51(1)
379-386
3
Allen E, Doisey E A.
Landmark article Sept. 8, 1923. An ovarian hormone: preliminary report on its localization, extraction and partial purification, and action in test animals.
JAMA.
1983;
250
2681-2683
4
Hisaw F L, Meyer R K, Weichert C K.
Inhibition of ovulation and associated histologic changes.
Proc Soc Exp Biol Med.
1928;
20
754-756
5
Hisaw F L, Leonard S L.
Production of a premenstrual endometrium in castrated monkeys by ovarian hormones.
Proc Soc Exp Biol Med.
1930;
27
400-403
6
Allen W M, Corner G W.
Physiology of the corpus luteum.
Am J Obstet Gynecol.
2005;
193
1574
7
Jensen E V, DeSombre E R.
Estrogen-receptor interaction.
Science.
1973;
182
126-134
8
Gorski J, Toft D, Shyamala G, Smith D, Notides A.
Hormone receptors: studies on the interaction of estrogen with the uterus.
Recent Prog Horm Res.
1968;
24
45-80
9
O'Malley B W, Sherman M R, Toft D O.
Progesterone “receptors” in the cytoplasm and nucleus of chick oviduct target tissue.
Proc Natl Acad Sci U S A.
1970;
67
501-508
10
O'Malley B W, Means A R.
Female steroid hormones and target cell nuclei.
Science.
1974;
183(125)
610-620
11
Mueller G C, Herranen A M, Jervell K F.
Studies on the mechanism of action of estrogens.
Recent Prog Horm Res.
1958;
14
95-129
discussion 130-129
12 Jensen E V. Proceedings of the 4th International Congress of Biochemistry Vol 15 Oxford, United Kingdom; Pergamon Press 1958
13 Jensen E V, Jacobson H I. Fate of steroid receptor estrogens in target tissues . In: Pincus G, Vollmer EP Biological Activities of Steroids in Relation to Cancer. New York, NY; Academic Press 1960
14
Jensen E V, DeSombre E R.
Estrogen-receptor interaction.
Science.
1973;
182
126-134
15
Lubahn D B, Moyer J S, Golding T S, Couse J F, Korach K S, Smithies O.
Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene.
Proc Natl Acad Sci U S A.
1993;
90(23)
11162-11166
16
Korach K S.
Insights from the study of animals lacking functional estrogen receptor.
Science.
1994;
266(5190)
1524-1527
17
Smith E P, Boyd J, Frank G R et al..
Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man.
N Engl J Med.
1994;
331(16)
1056-1061
18
Korach K S.
Insights from the study of animals lacking functional estrogen receptor.
Science.
1994;
266(5190)
1524-1527
19
Conneely O M, Mulac-Jericevic B, DeMayo F, Lydon J P, O'Malley B W.
Reproductive functions of progesterone receptors.
Recent Prog Horm Res.
2002;
57
339-355
20
Cooke P S, Buchanan D L, Lubahn D B, Cunha G R.
Mechanism of estrogen action: lessons from the estrogen receptor-α knockout mouse.
Biol Reprod.
1998;
59(3)
470-475
21
Kurita T, Lee K J, Cooke P S, Taylor J A, Lubahn D B, Cunha G R.
Paracrine regulation of epithelial progesterone receptor by estradiol in the mouse female reproductive tract.
Biol Reprod.
2000;
62(4)
821-830
22
Kurita T, Young P, Brody J R, Lydon J P, O'Malley B W, Cunha G R.
Stromal progesterone receptors mediate the inhibitory effects of progesterone on estrogen-induced uterine epithelial cell deoxyribonucleic acid synthesis.
Endocrinology.
1998;
139(11)
4708-4713
23
Milin B, Roy A K.
Androgen “receptor” in rat liver: cytosol “receptor” deficiency in pseudohermaphrodite male rats.
Nat New Biol.
1973;
242(121)
248-250
24
Brown T R, Lubahn D B, Wilson E M, Joseph D R, French F S, Migeon C J.
Deletion of the steroid-binding domain of the human androgen receptor gene in one family with complete androgen insensitivity syndrome: evidence for further genetic heterogeneity in this syndrome.
Proc Natl Acad Sci U S A.
1988;
85(21)
8151-8155
25 Erickson G F, Yen S SC. The polycystic ovary syndrome . In: Adashi EY, Leung PCK The Ovary. New York, NY; Raven Press 1993
26
Franks S.
Polycystic ovary syndrome.
Arch Dis Child.
1997;
77(1)
89-90
27
Homburg R.
Polycystic ovary syndrome.
Best Pract Res Clin Obstet Gynaecol.
2008;
22
261-274
28
Navaratnarajah R, Pillay O C, Hardiman P.
Polycystic ovary syndrome and endometrial cancer.
Semin Reprod Med.
2008;
26(1)
62-71
29 Fritz M A, Lessey B A. Defective luteal function . In: Fraser IS Estrogens and Progestogens in Clinical Practice. Vol 1. London, United Kingdom; Churchill Livingstone 1998
30
Jones G E.
Some newer aspects of the management of infertility.
J Am Med Assoc.
1949;
141
1123-1129
31
Burney R O, Talbi S, Hamilton A E et al..
Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis.
Endocrinology.
2007;
148(8)
3814-3826
32
Lessey B A, Killam A P, Metzger D A, Haney A F, Greene G L, McCarty Jr K S.
Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle.
J Clin Endocrinol Metab.
1988;
67(2)
334-340
33
Talbi S, Hamilton A E, Vo K C et al..
Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women.
Endocrinology.
2006;
147(3)
1097-1121
34
Catalano R D, Critchley H O, Heikinheimo O et al..
Mifepristone induced progesterone withdrawal reveals novel regulatory pathways in human endometrium.
Mol Hum Reprod.
2007;
13(9)
641-654
35
Joshi S G, Ebert K M, Smith R A.
Properties of the progestagen-dependent protein of the human endometrium.
J Reprod Fertil.
1980;
59(2)
287-296
36
Joshi S G, Ebert K M, Swartz D P.
Detection and synthesis of a progestagen-dependent protein in human endometrium.
J Reprod Fertil.
1980;
59(2)
273-285
37
Joshi S G.
Progestin-regulated proteins of the human endometrium.
Semin Reprod Endocrinol.
1983;
1
221
38
Julkunen M, Raikar R S, Joshi S G, Bohn H, Seppälä M.
Placental protein 14 and progestagen-dependent endometrial protein are immunologically indistinguishable.
Hum Reprod.
1986;
1(1)
7-8
39
Bohn H, Kraus W.
Isolation and characterization of a new placenta specific protein (PP12).
Arch Gynecol.
1980;
229
279-291
40
Rutanen E M, Koistinen R, Seppälä M, Julkunen M, Suikkari A M, Huhtala M L.
Progesterone-associated proteins PP12 and PP14 in the human endometrium.
J Steroid Biochem.
1987;
27(1-3)
25-31
41
Bischof P.
Three pregnancy proteins (PP12, PP14, and PAPP-A): their biological and clinical relevance.
Am J Perinatol.
1989;
6(2)
110-116
42
Julkunen M, Koistinen R, Sjöberg J, Rutanen E M, Wahlström T, Seppälä M.
Secretory endometrium synthesizes placental protein 14.
Endocrinology.
1986;
118(5)
1782-1786
43
Rutanen E M, Koistinen R, Sjöberg J et al..
Synthesis of placental protein 12 by human endometrium.
Endocrinology.
1986;
118(3)
1067-1071
44
Giudice L C, Lamson G, Rosenfeld R G, Irwin J C.
Insulin-like growth factor-II (IGF-II) and IGF binding proteins in human endometrium.
Ann N Y Acad Sci.
1991;
626
295-307
45
Seppälä M, Koistinen R, Rutanen E M.
Uterine endocrinology and paracrinology: insulin-like growth factor binding protein-1 and placental protein 14 revisited.
Hum Reprod.
1994;
9(5)
917-925
46
Rutanen E M, Pekonen F, Nyman T, Wahlström T.
Insulin-like growth factors and their binding proteins in benign and malignant uterine diseases.
Growth Regul.
1993;
3(1)
74-77
47
Giudice L C, Dsupin B A, Jin I H, Vu T H, Hoffman A R.
Differential expression of messenger ribonucleic acids encoding insulin-like growth factors and their receptors in human uterine endometrium and decidua.
J Clin Endocrinol Metab.
1993;
76(5)
1115-1122
48
Bell S C.
The insulin-like growth factor binding proteins—the endometrium and decidua.
Ann N Y Acad Sci.
1991;
622
120-137
49
Tseng L, Gao J G, Chen R, Zhu H H, Mazella J, Powell D R.
Effect of progestin, antiprogestin, and relaxin on the accumulation of prolactin and insulin-like growth factor-binding protein-1 messenger ribonucleic acid in human endometrial stromal cells.
Biol Reprod.
1992;
47(3)
441-450
50
Irwin J C, de las Fuentes L, Giudice L C.
Growth factors and decidualization in vitro.
Ann N Y Acad Sci.
1994;
734
7-18
51
Frost R A, Mazella J, Tseng L.
Insulin-like growth factor binding protein-1 inhibits the mitogenic effect of insulin-like growth factors and progestins in human endometrial stromal cells.
Biol Reprod.
1993;
49(1)
104-111
52
Irwin J C, Suen L F, Martina N A, Mark S P, Giudice L C.
Role of the IGF system in trophoblast invasion and pre-eclampsia.
Hum Reprod.
1999;
14(Suppl 2)
90-96
53
Li T C, Dalton C, Hunjan K S, Warren M A, Bolton A E.
The correlation of placental protein 14 concentrations in uterine flushing and endometrial morphology in the peri-implantation period.
Hum Reprod.
1993;
8(11)
1923-1927
54
Klentzeris L D, Bulmer J N, Seppälä M, Li T C, Warren M A, Cooke I D.
Placental protein 14 in cycles with normal and retarded endometrial differentiation.
Hum Reprod.
1994;
9(3)
394-398
55
Dalton C F, Laird S M, Serle E et al..
The measurement of CA 125 and placental protein 14 in uterine flushings in women with recurrent miscarriage; relation to endometrial morphology.
Hum Reprod.
1995;
10(10)
2680-2684
56
Oehninger S, Coddington C C, Hodgen G D, Seppala M.
Factors affecting fertilization: endometrial placental protein 14 reduces the capacity of human spermatozoa to bind to the human zona pellucida.
Fertil Steril.
1995;
63(2)
377-383
57
Clark G F, Oehninger S, Patankar M S et al..
A role for glycoconjugates in human development: the human feto-embryonic defence system hypothesis.
Hum Reprod.
1996;
11(3)
467-473
58
Karande A A, Mukhopadhyay D, Jayachandran R, Sundarraj S, Alok A.
Mechanism of the immunomodulatory activity of glycodelin.
Indian J Physiol Pharmacol.
2005;
49(3)
271-283
59
Alok A, Mukhopadhyay D, Karande A A.
Glycodelin A, an immunomodulatory protein in the endometrium, inhibits proliferation and induces apoptosis in monocytic cells.
Int J Biochem Cell Biol.
2009;
41(5)
1138-1147
60
Seppälä M, Taylor R N, Koistinen H, Koistinen R, Milgrom E.
Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation.
Endocr Rev.
2002;
23(4)
401-430
61
Stavreus-Evers A, Mandelin E, Koistinen R et al..
Glycodelin is present in pinopodes of receptive-phase human endometrium and is associated with down-regulation of progesterone receptor B.
Fertil Steril.
2006;
85(6)
1803-1811
62
Hasty L A, Lessey B A, Pruksananonda K et al..
The hormonal regulation of complement components throughout the menstrual cycle.
Proc of the Soc Gynecol Invest.
1992;
63
Hasty L A, Brockman W W, Lambris J D, Lyttle C R.
Hormonal regulation of complement factor B in human endometrium.
Am J Reprod Immunol.
1993;
30(2-3)
63-67
64
Hasty L A, Lambris J D, Lessey B A, Pruksananonda K, Lyttle C R.
Hormonal regulation of complement components and receptors throughout the menstrual cycle.
Am J Obstet Gynecol.
1994;
170(1 Pt 1)
168-175
65
Young S L, Lessey B A, Fritz M A et al..
In vivo and in vitro evidence suggest that HB-EGF regulates endometrial expression of human decay-accelerating factor.
J Clin Endocrinol Metab.
2002;
87(3)
1368-1375
66
Apparao K B, Murray M J, Fritz M A et al..
Osteopontin and its receptor alphavbeta(3) integrin are coexpressed in the human endometrium during the menstrual cycle but regulated differentially.
J Clin Endocrinol Metab.
2001;
86(10)
4991-5000
67
Lessey B A, Castelbaum A J.
Integrins and implantation in the human.
Rev Endocr Metab Disord.
2002;
3(2)
107-117
68
Fedarko N S, Fohr B, Robey P G, Young M F, Fisher L W.
Factor H binding to bone sialoprotein and osteopontin enables tumor cell evasion of complement-mediated attack.
J Biol Chem.
2000;
275(22)
16666-16672
69
Fisher L W, Torchia D A, Fohr B, Young M F, Fedarko N S.
Flexible structures of SIBLING proteins, bone sialoprotein, and osteopontin.
Biochem Biophys Res Commun.
2001;
280(2)
460-465
70
Jain A, Karadag A, Fohr B, Fisher L W, Fedarko N S.
Three SIBLINGs (small integrin-binding ligand, N-linked glycoproteins) enhance factor H's cofactor activity enabling MCP-like cellular evasion of complement-mediated attack.
J Biol Chem.
2002;
277(16)
13700-13708
71
Isaacson K B, Coutifaris C, Garcia C R, Lyttle C R.
Production and secretion of complement component 3 by endometriotic tissue.
J Clin Endocrinol Metab.
1989;
69(5)
1003-1009
72
Isaacson K B, Galman M, Coutifaris C, Lyttle C R.
Endometrial synthesis and secretion of complement component-3 by patients with and without endometriosis.
Fertil Steril.
1990;
53(5)
836-841
73
Tao X J, Sayegh R A, Isaacson K B.
Increased expression of complement component 3 in human ectopic endometrium compared with the matched eutopic endometrium.
Fertil Steril.
1997;
68(3)
460-467
74
Holers V M, Girardi G, Mo L et al..
Complement C3 activation is required for antiphospholipid antibody-induced fetal loss.
J Exp Med.
2002;
195(2)
211-220
75
Xu C, Mao D, Holers V M, Palanca B, Cheng A M, Molina H.
A critical role for murine complement regulator Crry in fetomaternal tolerance.
Science.
2000;
287(5452)
498-501
76
Molina H.
The murine complement regulator Crry: new insights into the immunobiology of complement regulation.
Cell Mol Life Sci.
2002;
59(2)
220-229
77
Jorgenson R L, Young S L, Lesmeister M J, Lyddon T D, Misfeldt M L.
Human endometrial epithelial cells cyclically express Toll-like receptor 3 (TLR3) and exhibit TLR3-dependent responses to dsRNA.
Hum Immunol.
2005;
66(5)
469-482
78
Fazeli A, Bruce C, Anumba D O.
Characterization of Toll-like receptors in the female reproductive tract in humans.
Hum Reprod.
2005;
20(5)
1372-1378
79
Schaefer T M, Desouza K, Fahey J V, Beagley K W, Wira C R.
Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells.
Immunology.
2004;
112(3)
428-436
80
Pioli P A, Amiel E, Schaefer T M, Connolly J E, Wira C R, Guyre P M.
Differential expression of Toll-like receptors 2 and 4 in tissues of the human female reproductive tract.
Infect Immun.
2004;
72(10)
5799-5806
81
Csapo A I, Pulkkinen M.
Indispensability of the human corpus luteum in the maintenance of early pregnancy. Luteectomy evidence.
Obstet Gynecol Surv.
1978;
33(2)
69-81
82
Baulieu E E.
Contragestion and other clinical applications of RU 486, an antiprogesterone at the receptor.
Science.
1989;
245(4924)
1351-1357
83
Baulieu E E.
RU486: a compound that gets itself talked about.
Hum Reprod.
1994;
9(Suppl 1)
1-6
84
Somkuti S G, Yuan L, Fritz M A, Lessey B A.
Epidermal growth factor and sex steroids dynamically regulate a marker of endometrial receptivity in Ishikawa cells.
J Clin Endocrinol Metab.
1997;
82(7)
2192-2197
85
Kurihara I, Lee D K, Petit F G et al..
COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity.
PLoS Genet.
2007;
3(6)
e102
86
Lessey B A.
Two pathways of progesterone action in the human endometrium: implications for implantation and contraception.
Steroids.
2003;
68(10-13)
809-815
87
Aplin J D, Charlton A K, Ayad S.
An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy.
Cell Tissue Res.
1988;
253(1)
231-240
88
Ruck P, Marzusch K, Kaiserling E et al..
Distribution of cell adhesion molecules in decidua of early human pregnancy. An immunohistochemical study.
Lab Invest.
1994;
71(1)
94-101
89
Turpeenniemi-Hujanen T, Feinberg R F, Kauppila A, Puistola U.
Extracellular matrix interactions in early human embryos: implications for normal implantation events.
Fertil Steril.
1995;
64(1)
132-138
90
Albelda S M, Buck C A.
Integrins and other cell adhesion molecules.
FASEB J.
1990;
4
2868-2880
91
Lessey B A, Damjanovich L, Coutifaris C, Castelbaum A, Albelda S M, Buck C A.
Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle.
J Clin Invest.
1992;
90(1)
188-195
92
Lessey B A, Castelbaum A J, Buck C A, Lei Y, Yowell C W, Sun J.
Further characterization of endometrial integrins during the menstrual cycle and in pregnancy.
Fertil Steril.
1994;
62(3)
497-506
93
Tabibzadeh S.
Patterns of expression of integrin molecules in human endometrium throughout the menstrual cycle.
Hum Reprod.
1992;
7(6)
876-882
94
Damsky C, Sutherland A, Fisher S.
Extracellular matrix 5: adhesive interactions in early mammalian embryogenesis, implantation, and placentation.
FASEB J.
1993;
7(14)
1320-1329
95
Armant D R, Kaplan H A, Mover H, Lennarz W J.
The effect of hexapeptides on attachment and outgrowth of mouse blastocysts cultured in vitro: evidence for the involvement of the cell recognition tripeptide Arg-Gly-Asp.
Proc Natl Acad Sci U S A.
1986;
83(18)
6751-6755
96
Illera M J, Cullinan E, Gui Y, Yuan L, Beyler S A, Lessey B A.
Blockade of the alpha(v)beta(3) integrin adversely affects implantation in the mouse.
Biol Reprod.
2000;
62(5)
1285-1290
97
Illera M J, Gui Y T, Mohammad A et al..
Perturbation of implantation rate by neutralization of the αvβ3 vitronectin receptor in rabbits.
J Soc Gynecol Invest.
1999;
379
143A
98
Bronson R A, Fusi F M.
Integrins and human reproduction.
Mol Hum Reprod.
1996;
2(3)
153-168
99
Yelian F D, Yang Y, Hirata J D, Schultz J F, Armant D R.
Molecular interactions between fibronectin and integrins during mouse blastocyst outgrowth.
Mol Reprod Dev.
1995;
41(4)
435-448
100
Jones J I, Gockerman A, Busby Jr W H, Wright G, Clemmons D R.
Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5 beta 1 integrin by means of its Arg-Gly-Asp sequence.
Proc Natl Acad Sci U S A.
1993;
90(22)
10553-10557
101
Schultz J F, Armant D R.
β 1- and β 3-class integrins mediate fibronectin binding activity at the surface of developing mouse peri-implantation blastocysts. Regulation by ligand-induced mobilization of stored receptor.
J Biol Chem.
1995;
270(19)
11522-11531
102
Yelian F D, Yang Y, Hirata J D, Schultz J F, Armant D R.
Molecular interactions between fibronectin and integrins during mouse blastocyst outgrowth.
Mol Reprod Dev.
1995;
41(4)
435-448
103
Illera M J, Lorenzo P L, Gui Y T, Beyler S A, Apparao K B, Lessey B A.
A role for alphavbeta3 integrin during implantation in the rabbit model.
Biol Reprod.
2003;
68(3)
766-771
104
Sutherland A E, Calarco P G, Damsky C H.
Developmental regulation of integrin expression at the time of implantation in the mouse embryo.
Development.
1993;
119(4)
1175-1186
105
Tseng L, Gurpide E.
Effects of progestins on estradiol receptor levels in human endometrium.
J Clin Endocrinol Metab.
1975;
41(2)
402-404
106
Bulun S E, Gurates B, Fang Z et al..
Mechanisms of excessive estrogen formation in endometriosis.
J Reprod Immunol.
2002;
55(1-2)
21-33
107
Noble L S, Simpson E R, Johns A, Bulun S E.
Aromatase expression in endometriosis.
J Clin Endocrinol Metab.
1996;
81(1)
174-179
108
Leon L, Bacallao K, Gabler F, Romero C, Valladares L, Vega M.
Activities of steroid metabolic enzymes in secretory endometria from untreated women with polycystic ovary syndrome.
Steroids.
2008;
73(1)
88-95
109
Kitawaki J, Noguchi T, Amatsu T et al..
Expression of aromatase cytochrome P450 protein and messenger ribonucleic acid in human endometriotic and adenomyotic tissues but not in normal endometrium.
Biol Reprod.
1997;
57(3)
514-519
110
Kitawaki J, Kusuki I, Koshiba H, Tsukamoto K, Honjo H.
Expression of aromatase cytochrome P450 in eutopic endometrium and its application as a diagnostic test for endometriosis.
Gynecol Obstet Invest.
1999;
48(Suppl 1)
21-28
111
Tranguch S, Cheung-Flynn J, Daikoku T et al..
Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation.
Proc Natl Acad Sci U S A.
2005;
102(40)
14326-14331
112
Tranguch S, Wang H, Daikoku T, Xie H, Smith D F, Dey S K.
FKBP52 deficiency-conferred uterine progesterone resistance is genetic background and pregnancy stage specific.
J Clin Invest.
2007;
117(7)
1824-1834
113
Usadi R S, Groll J M, Lessey B A et al..
Endometrial development and function in experimentally induced luteal phase deficiency.
J Clin Endocrinol Metab.
2008;
93(10)
4058-4064
114
Rock J, Bartlett M K.
Biopsy studies of human endometrium, criterion of dating and information about amenorrhea, menorrhagia, and tissue ovulation.
J Am Med Assoc.
1937;
108
2022-2028
115
Jones G E.
Some newer aspects of management of infertility.
J Am Med Assoc.
1949;
141
1123-1129
116
Noyes R W, Hertig A I, Rock J.
Dating the endometrial biopsy.
Fertil Steril.
1950;
1
3-25
117
Noyes R W, Haman J O.
Accuracy of endometrial dating; correlation of endometrial dating with basal body temperature and menses.
Fertil Steril.
1953;
4(6)
504-517
118 Castelbaum A J, Lessey B A. Insights into the evaluation of the luteal phase . In: Diamond MP Infertility and Reproductive Medicine. Vol 6. Philadelphia, PA; WB Saunders 1995: 199-213
119
Castelbaum A J, Wheeler J, Coutifaris C B, Mastroianni Jr L, Lessey B A.
Timing of the endometrial biopsy may be critical for the accurate diagnosis of luteal phase deficiency.
Fertil Steril.
1994;
61(3)
443-447
120
Murray M J, Meyer W R, Zaino R J et al..
A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women.
Fertil Steril.
2004;
81(5)
1333-1343
121
Scott R T, Snyder R R, Bagnall J W, Reed K D, Adair C F, Hensley S D.
Evaluation of the impact of intraobserver variability on endometrial dating and the diagnosis of luteal phase defects.
Fertil Steril.
1993;
60(4)
652-657
122
Coutifaris C, Myers E R, Guzick D S NICHD National Cooperative Reproductive Medicine Network et al.
Histological dating of timed endometrial biopsy tissue is not related to fertility status.
Fertil Steril.
2004;
82(5)
1264-1272
123
Castelbaum A J, Lessey B A.
Insights into the evaluation of the luteal phase.
Infert Reprod Med Clin No Am.
1994;
6
199
124
Soules M R, McLachlan R I, Ek M, Dahl K D, Cohen N L, Bremner W J.
Luteal phase deficiency: characterization of reproductive hormones over the menstrual cycle.
J Clin Endocrinol Metab.
1989;
69(4)
804-812
125
Li T C, Lenton E A, Dockery P, Cooke I D.
A comparison of some clinical and endocrinological features between cycles with normal and defective luteal phases in women with unexplained infertility.
Hum Reprod.
1990;
5(7)
805-810
126
Hecht B R, Bardawil W A, Khan-Dawood F S, Dawood M Y.
Luteal insufficiency: correlation between endometrial dating and integrated progesterone output in clomiphene citrate-induced cycles.
Am J Obstet Gynecol.
1990;
163(6 Pt 1)
1986-1991
127
Abraham G E, Maroulis G B, Marshall J R.
Evaluation of ovulation and corpus luteum function using measurements of plasma progesterone.
Obstet Gynecol.
1974;
44(4)
522-525
128
Hull M G, Savage P E, Bromham D R, Ismail A A, Morris A F.
The value of a single serum progesterone measurement in the midluteal phase as a criterion of a potentially fertile cycle (“ovulation”) derived form treated and untreated conception cycles.
Fertil Steril.
1982;
37(3)
355-360
129
Filicori M, Butler J P, Crowley Jr W F.
Neuroendocrine regulation of the corpus luteum in the human. Evidence for pulsatile progesterone secretion.
J Clin Invest.
1984;
73(6)
1638-1647
130
Nakajima S T, Gibson M.
Pathophysiology of luteal-phase deficiency in human reproduction.
Clin Obstet Gynecol.
1991;
34(1)
167-179
131
Wilcox A J, Baird D D, Weinberg C R.
Time of implantation of the conceptus and loss of pregnancy.
N Engl J Med.
1999;
340(23)
1796-1799
132
Wenner R.
Les antiprolactines.
Gynecologie.
1974;
25(2)
229-231
133
Franks S, Murray M AF, Jequier A M, Steele S J, Nabarro J D, Jacobs H S.
Incidence and significance of hyperprolactinaemia in women with amenorrhea.
Clin Endocrinol (Oxf).
1975;
4(6)
597-607
134
Corenblum B, Pairandeau N, Shewchuk A B.
Prolactin hypersecretion and short luteal phase defects.
Obstet Gynecol.
1976;
47
486-488
135
Spark R F, Pallotta J, Naftolin F, Clemens R.
Galactorrhea-amenorrhea syndromes: etiology and treatment.
Ann Intern Med.
1976;
84(5)
532-537
136
Mühlenstedt D, Bohnet H G, Hanker J P, Schneider H P.
Short luteal phase and prolactin.
Int J Fertil.
1978;
23(3)
213-218
137
del Pozo E, Wyss H, Tollis G, Alcañiz J, Campana A, Naftolin F.
Prolactin and deficient luteal function.
Obstet Gynecol.
1979;
53(3)
282-286
138
Edwards C RW, Forsyth I A, Besser G M.
Amenorrhoea, galactorrhoea, and primary hypothyroidism with high circulating levels of prolactin.
BMJ.
1971;
3(5772)
462-464
139
Daly D C, Walters C A, Soto-Albors C E, Riddick D H.
Endometrial biopsy during treatment of luteal phase defects is predictive of therapeutic outcome.
Fertil Steril.
1983;
40(3)
305-310
140
Sherman B M, Korenman S G.
Measurement of plasma LH, FSH, estradiol and progesterone in disorders of the human menstrual cycle: the short luteal phase.
J Clin Endocrinol Metab.
1974;
38(1)
89-93
141
Homburg R, Armar N A, Eshel A, Adams J, Jacobs H S.
Influence of serum luteinising hormone concentrations on ovulation, conception, and early pregnancy loss in polycystic ovary syndrome.
BMJ.
1988;
297(6655)
1024-1026
142
De Souza M J, Van Heest J, Demers L M, Lasley B L.
Luteal phase deficiency in recreational runners: evidence for a hypometabolic state.
J Clin Endocrinol Metab.
2003;
88(1)
337-346
143
Practice Committee of the American Society for Reproductive Medicine .
Progesterone supplementation during the luteal phase and in early pregnancy in the treatment of infertility: an educational bulletin.
Fertil Steril.
2008;
89(4)
789-792
144
Hubayter Z R, Muasher S J.
Luteal supplementation in in vitro fertilization: more questions than answers.
Fertil Steril.
2008;
89(4)
749-758
145
Daya S, Gunby J L.
WITHDRAWN: Luteal phase support in assisted reproduction cycles.
Cochrane Database Syst Rev.
2008;
(3)
CD004830
146
Keller D W, Wiest W G, Askin F B, Johnson L W, Strickler R C.
Pseudocorpus luteum insufficiency: a local defect of progesterone action on endometrial stroma.
J Clin Endocrinol Metab.
1979;
48(1)
127-132
147
McRae M A, Blasco L, Lyttle C R.
Serum hormones and their receptors in women with normal and inadequate corpus luteum function.
Fertil Steril.
1984;
42(1)
58-63
148
Abd-el-Maeboud K H, Eissa S, Kamel A S.
Altered endometrial progesterone/oestrogen receptor ratio in luteal phase defect.
Dis Markers.
1997;
13(2)
107-116
149
Ilesanmi A O, Hawkins D A, Lessey B A.
Immunohistochemical markers of uterine receptivity in the human endometrium.
Microsc Res Tech.
1993;
25(3)
208-222
150
Kliman H J, Honig S, Walls D, Luna M, McSweet J C, Copperman A B.
Optimization of endometrial preparation results in a normal endometrial function test (EFT) and good reproductive outcome in donor ovum recipients.
J Assist Reprod Genet.
2006;
23(7-8)
299-303
151
Wang B, Sheng J Z, He R H, Qian Y L, Jin F, Huang H F.
High expression of L-selectin ligand in secretory endometrium is associated with better endometrial receptivity and facilitates embryo implantation in human being.
Am J Reprod Immunol.
2008;
60(2)
127-134
152
Domínguez F, Remohí J, Pellicer A, Simón C.
Human endometrial receptivity: a genomic approach.
Reprod Biomed Online.
2003;
6(3)
332-338
153
Horcajadas J A, Pellicer A, Simón C.
Wide genomic analysis of human endometrial receptivity: new times, new opportunities.
Hum Reprod Update.
2007;
13(1)
77-86
154
Tapia A, Gangi L M, Zegers-Hochschild F et al..
Differences in the endometrial transcript profile during the receptive period between women who were refractory to implantation and those who achieved pregnancy.
Hum Reprod.
2008;
23(2)
340-351
155
Dey S K, Lim H, Das S K et al..
Molecular cues to implantation.
Endocr Rev.
2004;
25(3)
341-373
156
Donaghay M, Lessey B A.
Uterine receptivity: alterations associated with benign gynecological disease.
Semin Reprod Med.
2007;
25(6)
461-475
157
de los Santos M J, Mercader A, Galan A et al..
Implantation rates after two, three, or five days of embryo culture.
Placenta.
2003;
24(Suppl B)
13-19
158
Pope W F.
Uterine asynchrony: a cause of embryonic loss.
Biol Reprod.
1988;
39(5)
999-1003
159
Achache H, Revel A.
Endometrial receptivity markers, the journey to successful embryo implantation.
Hum Reprod Update.
2006;
12(6)
731-746
160
Aghajanova L, Hamilton A E, Giudice L C.
Uterine receptivity to human embryonic implantation: histology, biomarkers, and transcriptomics.
Semin Cell Dev Biol.
2008;
19(2)
204-211
161
Campbell K L, Rockett J C.
Biomarkers of ovulation, endometrial receptivity, fertilisation, implantation and early pregnancy progression.
Paediatr Perinat Epidemiol.
2006;
20(Suppl 1)
13-25
162
Cavagna M, Mantese J C.
Biomarkers of endometrial receptivity—a review.
Placenta.
2003;
24(Suppl B)
39-47
163
Haouzi D, Mahmoud K, Fourar M et al..
Identification of new biomarkers of human endometrial receptivity in the natural cycle.
Hum Reprod.
2009;
24(1)
198-205
164
Bell S C.
Secretory endometrial/decidual proteins and their function in early pregnancy.
J Reprod Fertil Suppl.
1988;
36
109-125
165
Heffner L J, Iddenden D A, Lyttle C R.
Electrophoretic analyses of secreted human endometrial proteins: identification and characterization of luteal phase prolactin.
J Clin Endocrinol Metab.
1986;
62(6)
1288-1295
166
Santoro N, MacLaughlin D T, Bauer H H, Hargraves A A, Dichek H L, Richardson G S.
In vitro protein production by the human endometrium.
Biol Reprod.
1989;
40(5)
1047-1055
167 Beier H M, Beier-Hellwig K, Sterzik S et al.. The significance of endometrial secretion proteins and their determination in human uterine secretions. In: Genazzani AR, Petraglia F Frontiers in Gynecologic and Obstetric Investigation. Carnforth, United Kingdom; Parthenon 1993
168 Beier-Hellwig K, Bonn B, Sterzik K et al.. Uterine receptivity and endometrial secretory protein patterns . In: Dey SK Molecular and Cellular Aspects of Preiimplantation Processes. Vol 1. New York, NY; Springer-Verlag 1995
169
Carson D D, Lagow E, Thathiah A et al..
Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening.
Mol Hum Reprod.
2002;
8(9)
871-879
170
Riesewijk A, Martín J, van Os R et al..
Gene expression profiling of human endometrial receptivity on days LH + 2 versus LH + 7 by microarray technology.
Mol Hum Reprod.
2003;
9(5)
253-264
171
Schmidt A, Groth P, Haendler B et al..
Gene expression during the implantation window: microarray analysis of human endometrial samples.
Ernst Schering Res Found Workshop.
2005;
(52)
139-157
172
Cowan B D, Hines R S, Brackin M N, Case S T.
Temporal and cell-specific gene expression by human endometrium after coculture with trophoblast.
Am J Obstet Gynecol.
1999;
180(4)
806-814
173
Haendler B, Yamanouchi H, Lessey B A, Chwalisz K, Hess-Stumpp H.
Cycle-dependent endometrial expression and hormonal regulation of the fibulin-1 gene.
Mol Reprod Dev.
2004;
68(3)
279-287
174
Tabibzadeh S, Sun X Z.
Cytokine expression in human endometrium throughout the menstrual cycle.
Hum Reprod.
1992;
7(9)
1214-1221
175
Somkuti S G, Yuan L, Fritz M A, Lessey B A.
Epidermal growth factor and sex steroids dynamically regulate a marker of endometrial receptivity in Ishikawa cells.
J Clin Endocrinol Metab.
1997;
82(7)
2192-2197
176
Daftary G S, Troy P J, Bagot C N, Young S L, Taylor H S.
Direct regulation of beta3-integrin subunit gene expression by HOXA10 in endometrial cells.
Mol Endocrinol.
2002;
16(3)
571-579
177
Apparao K B, Murray M J, Fritz M A et al..
Osteopontin and its receptor alphavbeta(3) integrin are coexpressed in the human endometrium during the menstrual cycle but regulated differentially.
J Clin Endocrinol Metab.
2001;
86(10)
4991-5000
178
Genbacev O D, Prakobphol A, Foulk R A et al..
Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface.
Science.
2003;
299(5605)
405-408
179
Lai T H, Zhao Y, Shih IeM, Ho C L, Bankowski B, Vlahos N.
Expression of L-selectin ligands in human endometrium during the implantation window after controlled ovarian stimulation for oocyte donation.
Fertil Steril.
2006;
85(3)
761-763
180
Foulk R A, Zdravkovic T, Genbacev O, Prakobphol A.
Expression of L-selectin ligand MECA-79 as a predictive marker of human uterine receptivity.
J Assist Reprod Genet.
2007;
24(7)
316-321
181
Kumar S, Zhu L J, Polihronis M et al..
Progesterone induces calcitonin gene expression in human endometrium within the putative window of implantation.
J Clin Endocrinol Metab.
1998;
83(12)
4443-4450
182
Zhu L J, Cullinan-Bove K, Polihronis M, Bagchi M K, Bagchi I C.
Calcitonin is a progesterone-regulated marker that forecasts the receptive state of endometrium during implantation.
Endocrinology.
1998;
139(9)
3923-3934
183
Li Q, Wang J, Armant D R, Bagchi M K, Bagchi I C.
Calcitonin down-regulates E-cadherin expression in rodent uterine epithelium during implantation.
J Biol Chem.
2002;
277(48)
46447-46455
184
Chen G TC, Getsios S, MacCalman C D.
Cadherin-11 is a hormonally regulated cellular marker of decidualization in human endometrial stromal cells.
Mol Reprod Dev.
1999;
52(2)
158-165
185
MacCalman C D, Furth E E, Omigbodun A, Bronner M, Coutifaris C, Strauss III J F.
Regulated expression of cadherin-11 in human epithelial cells: a role for cadherin-11 in trophoblast-endometrium interactions?.
Dev Dyn.
1996;
206(2)
201-211
186
Birdsall M A, Hopkisson J F, Grant K E, Barlow D H, Mardon H J.
Expression of heparin-binding epidermal growth factor messenger RNA in the human endometrium.
Mol Hum Reprod.
1996;
2(1)
31-34
187
Kimber S J.
Molecular interactions at the maternal-embryonic interface during the early phase of implantation.
Semin Reprod Med.
2000;
18(3)
237-253
188
Martin K L, Barlow D H, Sargent I L.
Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium.
Hum Reprod.
1998;
13(6)
1645-1652
189
Lessey B A, Gui Y, Apparao K B, Young S L, Mulholland J.
Regulated expression of heparin-binding EGF-like growth factor (HB-EGF) in the human endometrium: a potential paracrine role during implantation.
Mol Reprod Dev.
2002;
62(4)
446-455
Steven L YoungM.D. Ph.D.
Department of Obstetrics & Gynecology (CB# 7570)
4005 Old Clinic Bldg, University of North Carolina at Chapel Hill, Chapel Hill NC 27599-7570
eMail: youngs@med.unc.edu