Lack of functional pregnancy-associated plasma protein-A (PAPPA) compromises mouse ovarian steroidogenesis and female fertility

Biology of Reproduction

Volumn 82, Issue 6, 2010, Pages 1129-1138

  Nyegaard, Mette ^a,b,c   Overgaard, Michael T ^a,b,d   Su, You Qiang ^a,f   Hamilton, Amy E ^a,b   Kwintkiewicz, Jakub ^b   Hsieh, Minnie ^a,b   Nayak, Nihar R ^a   Conti, Marco ^a,b   Conover, Cheryl A ^e   Giudice, Linda C ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c AALBORG UNIVERSITY HOSPITAL   (Denmark)

^d AALBORG UNIVERSITY   (Denmark)

^e MAYO CLINIC   (United States)

^f JACKSON LABORATORY   (United States)

Author keywords

Follicle; Growth factors; Insulin like growth factor binding protein proteolysis; Mechanisms of hormone action; Ovary

Indexed keywords

CHORIONIC GONADOTROPIN; ESTRADIOL; LUTEINIZING HORMONE RECEPTOR; PREGNANCY ASSOCIATED PLASMA PROTEIN A; PROGESTERONE; SOMATOMEDIN; SOMATOMEDIN BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOAVAILABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; ESTRADIOL BLOOD LEVEL; FEMALE; FEMALE FERTILITY; GENE DELETION; GENE EXPRESSION; HETEROZYGOTE; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PROTEIN DEGRADATION; STEROIDOGENESIS;

ANIMALS; CHORIONIC GONADOTROPIN; ENDOPEPTIDASES; ESTRADIOL; FEMALE; GONADAL STEROID HORMONES; INFERTILITY, FEMALE; LITTER SIZE; MICE; MICE, KNOCKOUT; OOCYTES; OVARY; PREGNANCY-ASSOCIATED PLASMA PROTEIN-A; PROGESTERONE; RECEPTORS, FSH; RECEPTORS, LH;

EQUIDAE; MUS;

EID: 77953830549     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.079517     Document Type: Article

References (44)

1. Kwintkiewicz J, Giudice LC. The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function. Semin Reprod Med 2009; 27:43-51.
2. Dupont J, Dunn SE, Barrett JC, LeRoith D. Microarray analysis and identification of novel molecules involved in insulin-like growth factor-1 receptor signaling and gene expression. Recent Prog Horm Res 2003; 58:325-342.
3. Samani AA, Yakar S, LeRoith D, Brodt P. The role of the IGF system in cancer growth and metastasis: overview and recent insights. Endocr Rev 2007; 28:20-47.
4. Rose PP, Bogyo M, Moses AV, Fruh K. Insulin-like growth factor II receptor-mediated intracellular retention of cathepsin B is essential for transformation of endothelial cells by Kaposi's sarcoma-associated herpesvirus. J Virol 2007; 81:8050-8062.
5. Boldt HB, Conover CA. Pregnancy-associated plasma protein-A (PAPP-A): a local regulator of IGF bioavailability through cleavage of IGFBPs. Growth Horm IGF Res 2007; 17:10-18.
6. Clemmons DR. Role of insulin-like growth factor binding proteins in controlling IGF actions. Mol Cell Endocrinol 1998; 140:19-24.
7. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 1995; 16:3-34.
8. Cataldo NA, Giudice LC. Insulin-like growth factor binding protein profiles in human ovarian follicular fluid correlate with follicular functional status. J Clin Endocrinol Metab 1992; 74:821-829.
9. Chandrasekher YA, Van Dessel HJ, Fauser BC, Giudice LC. Estrogen- but not androgen-dominant human ovarian follicular fluid contains an insulin-like growth factor binding protein-4 protease. J Clin Endocrinol Metab 1995; 80:2734-2739.
10. Conover CA, Faessen GF, Ilg KE, Chandrasekher YA, Christiansen M, Overgaard MT, Oxvig C, Giudice LC. Pregnancy-associated plasma protein-a is the insulin-like growth factor binding protein-4 protease secreted by human ovarian granulosa cells and is a marker of dominant follicle selection and the corpus luteum. Endocrinology 2001; 142:2155.
11. Thierry van Dessel HJ, Chandrasekher Y, Yap OW, Lee PD, Hintz RL, Faessen GH, Braat DD, Fauser BC, Giudice LC. Serum and follicular fluid levels of insulin-like growth factor I (IGF-I), IGF-II, and IGF-binding protein-1 and -3 during the normal menstrual cycle. J Clin Endocrinol Metab 1996; 81:1224-1231. (Pubitemid 126423251)
12. Giudice LC. Insulin-like growth factor family in Graafian follicle development and function. J Soc Gynecol Investig 2001; 8:S26-S29.
13. Conover CA, Oxvig C, Overgaard MT, Christiansen M, Giudice LC. Evidence that the insulin-like growth factor binding protein-4 protease in human ovarian follicular fluid is pregnancy associated plasma protein-A. J Clin Endocrinol Metab 1999; 84:4742-4745.
14. Mazerbourg S, Overgaard MT, Oxvig C, Christiansen M, Conover CA, Laurendeau I, Vidaud M, Tosser-Klopp G, Zapf J, Monget P. Pregnancy-associated plasma protein-A (PAPP-A) in ovine, bovine, porcine, and equine ovarian follicles: involvement in IGF binding protein-4 proteolytic degradation and mRNA expression during follicular development. Endocrinology 2001; 142:5243-5253.
15. Monget P, Mazerbourg S, Delpuech T, Maurel MC, Maniere S, Zapf J, Lalmanach G, Oxvig C, Overgaard MT. Pregnancy-associated plasma protein-A is involved in insulin-like growth factor binding protein-2 (IGFBP-2) proteolytic degradation in bovine and porcine preovulatory follicles: identification of cleavage site and characterization of IGFBP-2 degradation. Biol Reprod 2003; 68:77-86.
16. Hourvitz A, Kuwahara A, Hennebold JD, Tavares AB, Negishi H, Lee TH, Erickson GF, Adashi EY. The regulated expression of the pregnancy-associated plasma protein-A in the rodent ovary: a proposed role in the development of dominant follicles and of corpora lutea. Endocrinology 2002; 143:1833-1844.
17. Hourvitz A, Widger AE, Filho FL, Chang RJ, Adashi EY, Erickson GF. Pregnancy-associated plasma protein-A gene expression in human ovaries is restricted to healthy follicles and corpora lutea. J Clin Endocrinol Metab 2000; 85:4916-4920.
18. Conover CA, Bale LK, Overgaard MT, Johnstone EW, Laursen UH, Fuchtbauer EM, Oxvig C, van Deursen J. Metalloproteinase pregnancy-associated plasma protein A is a critical growth regulatory factor during fetal development. Development 2004; 131:1187-1194.
19. Rankin TL, O'Brien M, Lee E, Wigglesworth K, Eppig J, Dean J. Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development. Development 2001; 128:1119-1126. (Pubitemid 32401427)
20. Talbi S, Hamilton AE, Vo KC, Tulac S, Overgaard MT, Dosiou C, Le Shay N, Nezhat CN, Kempson R, Lessey BA, Nayak NR, Giudice LC. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 2006; 147:1097-1121.
21. Jo Y, King SR, Khan SA, Stocco DM. Involvement of protein kinase C and cyclic adenosine 3′,5′-monophosphate-dependent kinase in steroidogenic acute regulatory protein expression and steroid biosynthesis in Leydig cells. Biol Reprod 2005; 73:244-255.
22. Mizuyachi K, Son DS, Rozman KK, Terranova PF. Alteration in ovarian gene expression in response to 2,3,7,8-tetrachlorodibenzo-p-dioxin: reduction of cyclooxygenase-2 in the blockage of ovulation. Reprod Toxicol 2002; 16:299-307.
23. Su YQ, Nyegaard M, Overgaard MT, Qiao J, Giudice LC. Participation of mitogen-activated protein kinase in luteinizing hormone-induced differential regulation of steroidogenesis and steroidogenic gene expression in mural and cumulus granulosa cells of mouse preovulatory follicles. Biol Reprod 2006; 75:859-867.
24. Laursen LS, Overgaard MT, Soe R, Boldt HB, Sottrup-Jensen L, Giudice LC, Conover CA, Oxvig C. Pregnancy-associated plasma protein-A (PAPP-A) cleaves insulin-like growth factor binding protein (IGFBP)-5 independent of IGF: implications for the mechanism of IGFBP-4 proteolysis by PAPP-A. FEBS Lett 2001; 504:36-40.
25. Boldt HB, Overgaard MT, Laursen LS, Weyer K, Sottrup-Jensen L, Oxvig C. Mutational analysis of the proteolytic domain of pregnancy-associated plasma protein-A (PAPP-A): classification as a metzincin. Biochem J 2001; 358:359-367.
26. Overgaard MT, Haaning J, Boldt HB, Olsen IM, Laursen LS, Christiansen M, Gleich GJ, Sottrup-Jensen L, Conover CA, Oxvig C. Expression of recombinant human pregnancy-associated plasma protein-A and identification of the proform of eosinophil major basic protein as its physiological inhibitor. J Biol Chem 2000; 275:31128-31133.
27. Jo M, Gieske MC, Payne CE, Wheeler-Price SE, Gieske JB, Ignatius IV, Curry TE Jr, Ko C. Development and application of a rat ovarian gene expression database. Endocrinology 2004; 145:5384-5396.
28. Laursen LS, Overgaard MT, Nielsen CG, Boldt HB, Hopmann KH, Conover CA, Sottrup-Jensen L, Giudice LC, Oxvig C. Substrate specificity of the metalloproteinase pregnancy-associated plasma protein-A (PAPP-A) assessed by mutagenesis and analysis of synthetic peptides: substrate residues distant from the scissile bond are critical for proteolysis. Biochem J 2002; 367:31-40.
29. Richards JS. Ovulation: new factors that prepare the oocyte for fertilization. Mol Cell Endocrinol 2005; 234:75-79.
30. Overgaard MT, Oxvig C, Christiansen M, Lawrence JB, Conover CA, Gleich GJ, Sottrup-Jensen L, Haaning J. Messenger ribonucleic acid levels of pregnancy-associated plasma protein-A and the proform of eosinophil major basic protein: expression in human reproductive and nonreproductive tissues. Biol Reprod 1999; 61:1083-1089.
31. Soe R, Overgaard MT, Thomsen AR, Laursen LS, Olsen IM, Sottrup-Jensen L, Haaning J, Giudice LC, Conover CA, Oxvig C. Expression of recombinant murine pregnancy-associated plasma protein-A (PAPP-A) and a novel variant (PAPP-Ai) with differential proteolytic activity. Eur J Biochem 2002; 269:2247-2256.
32. Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellve AR, Efstratiadis A. Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 1996; 10:903-918. (Pubitemid 26236351)
33. Liu JL, Yakar S, LeRoith D. Conditional knockout of mouse insulin-like growth factor-1 gene using the Cre/loxP system. Proc Soc Exp Biol Med 2000; 223:344-351. (Pubitemid 30180781)
34. Dierich A, Sairam MR, Monaco L, Fimia GM, Gansmuller A, LeMeur M, Sassone-Corsi P. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci U S A 1998; 95:13612-13617.
35. Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG, Charlton HM. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 2000; 141:1795-1803.
36. Fan HY, Liu Z, Shimada M, Sterneck E, Johnson PF, Hedrick SM, Richards JS. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 2009; 324:938-941.
37. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004; 303:682-684.
38. Matsui M, Sonntag B, Hwang SS, Byerly T, Hourvitz A, Adashi EY, Shimasaki S, Erickson GF. Pregnancy-associated plasma protein - a production in rat granulosa cells: stimulation by follicle-stimulating hormone and inhibition by the oocyte-derived bone morphogenetic protein-15. Endocrinology 2004; 145:3686-3695.
39. Aad PY, Voge JL, Santiago CA, Malayer JR, Spicer LJ. Real-time RT-PCR quantification of pregnancy-associated plasma protein-A mRNA abundance in bovine granulosa and theca cells: effects of hormones in vitro. Domest Anim Endocrinol 2006; 31:357-372.
40. Bunn RC, Fowlkes JL. Insulin-like growth factor binding protein proteolysis. Trends Endocrinol Metab 2003; 14:176-181.
41. Miller BS, Bronk JT, Nishiyama T, Yamagiwa H, Srivastava A, Bolander ME, Conover CA. Pregnancy associated plasma protein-A is necessary for expeditious fracture healing in mice. J Endocrinol 2007; 192:505-513.
42. Resch ZT, Simari RD, Conover CA. Targeted disruption of the pregnancy-associated plasma protein-A gene is associated with diminished smooth muscle cell response to insulin-like growth factor-I and resistance to neointimal hyperplasia after vascular injury. Endocrinology 2006; 147:5634-5640.
43. Ochsner SA, Russell DL, Day AJ, Breyer RM, Richards JS. Decreased expression of tumor necrosis factor-alpha-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice. Endocrinology 2003; 144:1008-1019.
44. Elvin JA, Clark AT, Wang P, Wolfman NM, Matzuk MM. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol 1999; 13:1035-1048. (Pubitemid 30645319)