Different protein expression patterns associated with polycystic ovary syndrome in human follicular fluid during controlled ovarian hyperstimulation
Guo Dai A D and Guangxiu Lu A B C E
+ Author Affiliations
- Author Affiliations
A Institute of Reproductive and Stem Cell Engineering, Central South University, Xiangya Road 84, Changsha 410078, People’s Republic of China.
B Reproductive and Genetic Hospital of CITIC-XIANGYA, Xiangya Road 84, Changsha 410078, People’s Republic of China.
C National Engineering and Research Center of Human Stem Cell, Xiangya Road 84, Changsha 410078, People’s Republic of China.
D College of Life Science, Hunan Normal University, Lushan Road 36, Changsha 410081, People’s Republic of China.
E Corresponding author. Email: lugxdirector@yahoo.com.cn
Reproduction, Fertility and Development 24(7) 893-904 https://doi.org/10.1071/RD11201
Submitted: 10 August 2011 Accepted: 16 January 2012 Published: 9 March 2012
Abstract
Polycystic ovary syndrome (PCOS) is one of the most common causes of anovulatory infertility, affecting 5–10% of females during their reproductive life. Currently the pathology of PCOS is largely unknown. To identify the differential protein expression in follicular fluids from PCOS and normal subjects during controlled ovarian hyperstimulation, we performed an initial proteomic study including two-dimensional gel electrophoresis (2DE) analysis and mass spectroscopy, and confirmed results by western blot. Thirty-two protein spots were shown to be significantly differentially expressed between PCOS and normal follicular fluids, of which 20 unique proteins were identified to be associated with cellular metabolism and physiological processes; 13 of these proteins were upregulated while seven were downregulated in PCOS follicular fluids. Western blotting analyses confirmed the differential expressions for three randomly selected proteins, i.e. upregulated α1-antitrypsin, apolipoprotein A-I and transferrin in follicular fluid from PCOS patients than normal controls. Furthermore, semiquantitative reverse transcription-polymerase chain reaction (RT–PCR) analyses revealed that mRNA levels of serine palmitoyltransferase 2, serine/threonine-protein kinase male germ cell-associated kinase (MAK) and DNA damage-regulated autophagy modulator protein 2 decreased significantly in granulosa cells of PCOS patients compared with normal samples. These results increase our understanding of PCOS and the identified genes may serve as candidate biomarkers to develop diagnostic and therapeutic tools.
Additional keywords: 2DE, ART, COH, IVF-ET, PCOS, proteome.
References
Aleporou-Marinou, V., Pappa, H., Marinou, H., Yalouris, P., and Patargias, T. (2002). Presence of alpha1-antitrypsin and transferrin in human follicular fluid – correlation with fertilisation. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 133, 105–111.| Presence of alpha1-antitrypsin and transferrin in human follicular fluid – correlation with fertilisation.Crossref | GoogleScholarGoogle Scholar | 12223217PubMed |
Anahory, T., Dechaud, H., Bennes, R., Marin, P., Lamb, N. J., and Laoudj, D. (2002). Identification of new proteins in follicular fluid of mature human follicles. Electrophoresis 23, 1197–1202.
| Identification of new proteins in follicular fluid of mature human follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs12qsLk%3D&md5=4204ee49d143997397951cc4d4f63a47CAS | 11981869PubMed |
Angelucci, S., Ciavardelli, D., Di Giuseppe, F., Eleuterio, E., Sulpizio, M., Tiboni, G. M., Giampietro, F., Palumbo, P., and Di Ilio, C. (2006). Proteome analysis of human follicular fluid. Biochim. Biophys. Acta 1764, 1775–1785.
| 1:CAS:528:DC%2BD28Xht1Sjs7zI&md5=40d0041f51b2c5cacc202f85c228147dCAS | 17067859PubMed |
Beck, F. K., and Rosenthal, T. C. (2002). Prealbumin: a marker for nutritional evaluation. Am. Fam. Physician 65, 1575–1578.
| 11989633PubMed |
Bjellqvist, B., Sanchez, J. C., Pasquali, C., Ravier, F., Paquet, N., Frutiger, S., Hughes, G. J., and Hochstrasser, D. (1993). Micropreparative two-dimensional electrophoresis allowing the separation of samples containing milligram amounts of proteins. Electrophoresis 14, 1375–1378.
| Micropreparative two-dimensional electrophoresis allowing the separation of samples containing milligram amounts of proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhtVWjtL0%3D&md5=1cb3e3c3fdf018f9294409d91b4b60f2CAS | 8137805PubMed |
Borro, M., Gentile, G., Stigliano, A., Misiti, S., Toscano, V., and Simmaco, M. (2007). Proteomic analysis of peripheral T lymphocytes, suitable circulating biosensors of strictly related diseases. Clin. Exp. Immunol. 150, 494–501.
| Proteomic analysis of peripheral T lymphocytes, suitable circulating biosensors of strictly related diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVOqtw%3D%3D&md5=6f319b50d550f6332223903d4b7a4b5cCAS | 17900306PubMed |
Brozinick, J. T. (2001). GLUT4 overexpression in db/db mice dose-dependently ameliorates diabetes but is not a lifelong cure. Diabetes 50, 593–600.
| GLUT4 overexpression in db/db mice dose-dependently ameliorates diabetes but is not a lifelong cure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslGgs74%3D&md5=1301135b8f799a71409c6f02296c8b58CAS | 11246879PubMed |
Burghen, G. A., Givens, J. R., and Kitabchi, A. E. (1980). Correlation of hyperandrogenism with hyperinsulinism in polycystic ovarian disease. J. Clin. Endocrinol. Metab. 50, 113–116.
| Correlation of hyperandrogenism with hyperinsulinism in polycystic ovarian disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c%2Fnt1eltA%3D%3D&md5=412d242a4d20140ab0c27c32d0180a8cCAS | 7350174PubMed |
Chlon, T. M., Taffany, D. A., Welsh, J., and Rowling, M. J. (2008). Retinoids modulate expression of the endocytic partners megalin, cubilin, and disabled-2 and uptake of vitamin D-binding protein in human mammary cells. J. Nutr. 138, 1323–1328.
| 1:CAS:528:DC%2BD1cXnsVOltLc%3D&md5=ab8ee59e0686f8a20b6cbc35414f90b1CAS | 18567755PubMed |
Clavero, A., Castilla, J. A., and Martinez, L. (2004). Expression of integrin fraction and adhesion molecules on human granulosa cells and its relation with oocyte maturity and follicular steroidogenesis. J. Assist. Reprod. Genet. 21, 187–195.
| Expression of integrin fraction and adhesion molecules on human granulosa cells and its relation with oocyte maturity and follicular steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2crlsFeguw%3D%3D&md5=c55c934f8803b92b908722a83e257be1CAS | 15526973PubMed |
Cortón, M., Botella-Carretero, J. I., López, J. A., Camafeita, E., San Millán, J. L., Escobar-Morreale, H. F., and Peral, B. (2008). Proteomic analysis of human omental adipose tissue in the polycystic ovary syndrome using two-dimensional difference gel electrophoresis and mass spectrometry. Hum. Reprod. 23, 651–661.
| Proteomic analysis of human omental adipose tissue in the polycystic ovary syndrome using two-dimensional difference gel electrophoresis and mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 18156650PubMed |
Estes, S. J., Ye, B., Qiu, W., Cramer, D., Hornstein, M. D., and Missmer, S. A. (2009). A proteomic analysis of IVF follicular fluid in women ≤32 years old. Fertil. Steril. 92, 1569–1578.
| A proteomic analysis of IVF follicular fluid in women ≤32 years old.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslKktQ%3D%3D&md5=7b0a24ab702aff06c81a0ca8c1ff9696CAS | 18980758PubMed |
Fahiminiya, S., Labas, V., Dacheux, J. L., and Gérard, N. (2011). Improvement of 2D-PAGE resolution of human, porcine and equine follicular fluid by means of hexapeptide library. Reprod. Domest. Anim. 46, 561–563.
| Improvement of 2D-PAGE resolution of human, porcine and equine follicular fluid by means of hexapeptide library.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotVGru7k%3D&md5=6df1e4cb3809849e4fcb074fe02361d2CAS | 20723137PubMed |
Ferrero, S., Gillott, D. J., Remorgida, V., Anserini, P., Ragni, N., and Grudzinskas, J. G. (2009). Proteomic analysis of peritoneal fluid in fertile and infertile women with endometriosis. J. Reprod. Med. 54, 32–40.
| 1:CAS:528:DC%2BD1MXls1yrs7s%3D&md5=85c6d1966f2824dd94f50bd8cebdc37bCAS | 19263878PubMed |
Friedrichs, W. E., Navarijo-Ashbaugh, A. L., Bowman, B. H., and Yang, F. (1995). Expression and inflammatory regulation of haptoglobin gene in adipocytes. Biochem. Biophys. Res. Commun. 209, 250–256.
| Expression and inflammatory regulation of haptoglobin gene in adipocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkvFyjsro%3D&md5=a20fc16b0f60fd80a72d4ba3a04703d9CAS | 7726843PubMed |
Gomme, P. T., and Bertolini, J. (2004). Therapeutic potential of vitamin D-binding protein. Trends Biotechnol. 22, 340–345.
| Therapeutic potential of vitamin D-binding protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1WktbY%3D&md5=238f0f312ada7ee8d7e251b320244c09CAS | 15245906PubMed |
Goudas, V. T., and Dumesic, D. A. (1997). Polycystic ovary syndrome. Endocrinol. Metab. Clin. North Am. 26, 893–912.
| Polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FptFKquw%3D%3D&md5=fda72a35b7178f9b5575bf6ba9810b66CAS | 9429864PubMed |
Gruemmer, R., Klein-Hitpass, L., and Neulen, J. (2005). Regulation of gene expression in endothelial cells: the role of human follicular fluid. J. Mol. Endocrinol. 34, 37–46.
| Regulation of gene expression in endothelial cells: the role of human follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1Kmt7k%3D&md5=309caa781c3e3add0888f959c9399369CAS | 15691876PubMed |
Gruys, E., Toussaint, M. J., Niewold, T. A., and Koopmans, S. J. (2005). Acute phase reaction and acute phase proteins. J. Zhejiang Univ. Sci. 6, 1045–1056.
| Acute phase reaction and acute phase proteins.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MrnsVSgsQ%3D%3D&md5=386d0defb0ab5f7eb687a37990fe00b5CAS |
Guzick, D. S. (2004). Polycystic ovary syndrome. Obstet. Gynecol. 103, 181–193.
| Polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOntr0%3D&md5=ba2d84fcf639009c31410d66d5c3f6fdCAS | 14704263PubMed |
Hassan, M. I., Waheed, A., Yadav, S., Singh, T. P., and Ahmad, F. (2008). Zinc alpha 2-glycoprotein: a multidisciplinary protein. Mol. Cancer Res. 6, 892–906.
| Zinc alpha 2-glycoprotein: a multidisciplinary protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVKhurk%3D&md5=47c7d9d70aa77dac7c71f93cc8254497CAS | 18567794PubMed |
Heijnen, E. M., Eijkemans, M. J., Hughes, E. G., Laven, J. S., Macklon, N. S., and Fauser, B. C. (2006). A meta-analysis of outcomes of conventional IVF in women with polycystic ovary syndrome. Hum. Reprod. Update 12, 13–21.
| A meta-analysis of outcomes of conventional IVF in women with polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnmslSgsw%3D%3D&md5=5586bce338a7055c59177d4b2098c91cCAS | 16123051PubMed |
Hyka, N., Dayer, J. M., Modoux, C., Kohno, T., Edwards, C. K., Roux-Lombard, P., and Burger, D. (2001). Apolipoprotein A-I inhibits the production of interleukin-1β and tumor necrosis factor-α by blocking contact-mediated activation of monocytes by T lymphocytes. Blood 97, 2381–2389.
| Apolipoprotein A-I inhibits the production of interleukin-1β and tumor necrosis factor-α by blocking contact-mediated activation of monocytes by T lymphocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivFOgtb4%3D&md5=913f7642d357fda9715bb490f219a3f6CAS | 11290601PubMed |
Jinno, A., Tanaka, K., Matsushime, H., Haneji, T., and Shibuya, M. (1993). Testis-specific mak protein kinase is expressed specifically in the meiotic phase in spermatogenesis and is associated with a 210-kilodalton cellular phosphoprotein. Mol. Cell Biol. 13, 4146–4156.
| 1:CAS:528:DyaK3sXltlKgsb0%3D&md5=5c9f37ab0db12ef17deff0314f5fd8b8CAS | 8321219PubMed |
Jungblut, P., and Thiede, B. (1997). Protein identification from 2-DE gels by MALDI mass spectrometry. Mass Spectrom. Rev. 16, 145–162.
| Protein identification from 2-DE gels by MALDI mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvFOhsL8%3D&md5=eeccd299f1fb3f579b74eaaffaec294cCAS | 9414492PubMed |
Jungheim, E. S., Lanzendorf, S. E., Odem, R. R., Moley, K. H., Chang, A. S., and Ratts, V. S. (2009). Morbid obesity is associated with lower clinical pregnancy rates after in vitro fertilisation in women with polycystic ovary syndrome. Fertil. Steril. 92, 256–261.
| 18692801PubMed |
Kahn, P. (1995). From genome to proteome: looking at a cell’s proteins. Science 270, 369–370.
| From genome to proteome: looking at a cell’s proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovVektLo%3D&md5=f2c93613e0825b45d8a3510c3e3079eaCAS | 7569989PubMed |
Kawano, Y., Narahara, H., Miyamura, K., Mifune, K., and Miyakawa, I. (1995). Inhibitory effect of transferrin on progesterone production in the granulosa cell of humans in vivo and porcine granulosa cell in vitro. Gynecol. Obstet. Invest. 40, 1–4.
| Inhibitory effect of transferrin on progesterone production in the granulosa cell of humans in vivo and porcine granulosa cell in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsFOgtb0%3D&md5=9ab91e40eeb67a2e97383ce4c230fdfeCAS | 7557634PubMed |
Kawano, Y., Fukuda, J., Nasu, K., Nishida, M., Narahara, H., and Miyakawa, I. (2004). Production of macrophage inflammatory protein-3alpha in human follicular fluid and cultured granulosa cells. Fertil. Steril. 82, 1206–1211.
| Production of macrophage inflammatory protein-3alpha in human follicular fluid and cultured granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitFCqs7w%3D&md5=7b5b1f681ee82af768d59d9091dfa7f2CAS | 15474097PubMed |
Kim, Y. S., Kim, M. S., Lee, S. H., Choi, B. C., Lim, J. M., Cha, K. Y., and Baek, K. H. (2006). Proteomic analysis of recurrent spontaneous abortion: identification of an inadequately expressed set of proteins in human follicular fluid. Proteomics 6, 3445–3454.
| Proteomic analysis of recurrent spontaneous abortion: identification of an inadequately expressed set of proteins in human follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1artb8%3D&md5=5fdfc2533a95d5b0daf27375ba8e88e2CAS | 16637005PubMed |
Klöting, N., Graham, T. E., Berndt, J., Kralisch, S., Kovacs, P., Wason, C. J., Fasshauer, M., Schön, M. R., Stumvoll, M., Blüher, M., and Kahn, B. B. (2007). Serum retinol-binding protein is more highly expressed in visceral than in subcutaneous adipose tissue and is a marker of intra-abdominal fat mass. Cell Metab. 6, 79–87.
| Serum retinol-binding protein is more highly expressed in visceral than in subcutaneous adipose tissue and is a marker of intra-abdominal fat mass.Crossref | GoogleScholarGoogle Scholar | 17618858PubMed |
Langlois, M. R., and Delanghe, J. R. (1996). Biological and clinical significance of haptoglobin polymorphism in humans. Clin. Chem. 42, 1589–1600.
| 1:CAS:528:DyaK28Xmt1eqs70%3D&md5=31be360337568a29cd19da1afff85de6CAS | 8855140PubMed |
Lee, H. C., Lee, S. W., Lee, K. W., Lee, S. W., Cha, K. Y., Kim, K. H., and Lee, S. (2005). Identification of new proteins in follicular fluid from mature human follicles by direct sample rehydration method of two-dimensional polyacrylamide gel electrophoresis. J. Korean Med. Sci. 20, 456–460.
| Identification of new proteins in follicular fluid from mature human follicles by direct sample rehydration method of two-dimensional polyacrylamide gel electrophoresis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1eiuro%3D&md5=d584cf9f73b9a9f8a71fc1726a1306bbCAS | 15953869PubMed |
Li, W., Zhang, B., and Tang, J. (2007). Sirtuin 2, a mammalian homolog of yeast silent information regulator-2 longevity regulator, is an oligodendroglial protein that decelerates cell differentiation through deacetylating α-tubulin. J. Neurosci. 27, 2606–2616.
| Sirtuin 2, a mammalian homolog of yeast silent information regulator-2 longevity regulator, is an oligodendroglial protein that decelerates cell differentiation through deacetylating α-tubulin.Crossref | GoogleScholarGoogle Scholar | 17344398PubMed |
Lominadze, D., and Dean, W. (2002). Involvement of fibrinogen specific binding in erythrocyte aggregation. Clin. Exp. Hypertens. 517, 41–44.
| 1:CAS:528:DC%2BD38XjtVamsb0%3D&md5=af1df18334efe354cd8ff5b3f29f6f3aCAS |
Lominadze, D., Dean, W. L., Tyagi, S. C., and Roberts, A. M. (2010). Mechanisms of fibrinogen-induced microvascular dysfunction during cardiovascular disease. Acta Physiol. (Oxf.) 198, 1–13.
| Mechanisms of fibrinogen-induced microvascular dysfunction during cardiovascular disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1Wm&md5=33aae196a562c175bf548118c41d99adCAS |
Long, X., Peng, C., and Lu, G. (2009). Isolation and identification of genes differentially expressed in premature luteinisation granulosa cell during controlled ovarian hyperstimulation. Fertil. Steril. 92, 1767–1771.
| Isolation and identification of genes differentially expressed in premature luteinisation granulosa cell during controlled ovarian hyperstimulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslKqug%3D%3D&md5=8ff0210797437fc029a554e2ca603f5cCAS | 19616208PubMed |
Ma, X., Fan, L., Meng, Y., Hou, Z., Mao, Y. D., Wang, W., Ding, W., and Liu, J. Y. (2007). Proteomic analysis of human ovaries from normal and polycystic ovarian syndrome. Mol. Hum. Reprod. 13, 527–535.
| Proteomic analysis of human ovaries from normal and polycystic ovarian syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos12jsbs%3D&md5=921608240ee2f0c987f26a820c65b7f6CAS | 17557764PubMed |
Matharoo-Ball, B., Hughes, C., Lancashire, L., Tooth, D., Ball, G., Creaser, C., Elgasim, M., Rees, R., Layfield, R., and Atiomo, W. (2007). Characterisation of biomarkers in PCOS using multiple distinct proteomic platforms. J. Proteome Res. 6, 3321–3328.
| Characterisation of biomarkers in PCOS using multiple distinct proteomic platforms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVCqu7w%3D&md5=6a2e60b48b85b6d7ad611572cb379132CAS | 17602513PubMed |
Mendoza, C., Ruiz-Requena, E., Ortega, E., Cremades, N., Martinez, F., Bernabeu, R., Greco, E., and Tesarik, J. (2002). Follicular fluid markers of oocyte developmental potential. Hum. Reprod. 17, 1017–1022.
| Follicular fluid markers of oocyte developmental potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs12isLk%3D&md5=5022fa7b794a5f7e20386d07ad7b779eCAS | 11925399PubMed |
Mulik, R. S., Mönkkönen, J., Juvonen, R. O., Mahadik, K. R., and Paradkar, A. R. (2010). Transferrin mediated solid lipid nanoparticles containing curcumin: enhanced in vitro anticancer activity by induction of apoptosis. Int. J. Pharm. 398, 190–203.
| Transferrin mediated solid lipid nanoparticles containing curcumin: enhanced in vitro anticancer activity by induction of apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWhtLvO&md5=78e4580534fd8974b0721958546fa789CAS | 20655375PubMed |
Ng, E. H. Y., Tang, O. S., and Ho, P. C. (2000). The significance of the number of antral follicles prior to stimulation in predicting ovarian responses in an IVF programme. Hum. Reprod. 15, 1937–1942.
| The significance of the number of antral follicles prior to stimulation in predicting ovarian responses in an IVF programme.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvot12rsg%3D%3D&md5=3d4bbd77d48deb67b720d022a5bde804CAS |
North, B. J., Marshall, B. L., Borra, M. T., Denu, J. M., and Verdin, E. (2003). The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol. Cell 11, 437–444.
| The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1Wgs7c%3D&md5=f3c79440837a3ec0816bb7e239cac4e9CAS | 12620231PubMed |
O’Prey, J., Skommer, J., Wilkinson, S., and Ryan, K. M. (2009). Analysis of DRAM-related proteins reveals evolutionarily conserved and divergent roles in the control of autophagy. Cell Cycle 8, 2260–2265.
| Analysis of DRAM-related proteins reveals evolutionarily conserved and divergent roles in the control of autophagy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslKgtLo%3D&md5=49f8319f117646819284c731d5bcdb40CAS | 19556885PubMed |
Park, S. M., Kim, K., and Lee, E. J. (2009). Reduced expression of DRAM2/TMEM77 in tumor cells interferes with cell death. Biochem. Biophys. Res. Commun. 390, 1340–1344.
| Reduced expression of DRAM2/TMEM77 in tumor cells interferes with cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2ksrfP&md5=5cee99ad872ba072beaa355f92308d74CAS | 19895784PubMed |
Reaven, G. M. (1993). Role of insulin resistance in the pathophysiology of non-insulin dependent diabetes mellitus. Diabetes Metab. Rev. 9, 5S–12S.
| Role of insulin resistance in the pathophysiology of non-insulin dependent diabetes mellitus.Crossref | GoogleScholarGoogle Scholar | 8299489PubMed |
Refai, E., Dekki, N., Yang, S. N., Imreh, G., Cabrera, O., Yu, L., Yang, G., Norgren, S., Rössner, S. M., Inverardi, L., Ricordi, C., Olivecrona, G., Andersson, M., Jörnvall, H., Berggren, P. O., and Juntti-Berggren, L. (2005). Transthyretin constitutes a functional component in pancreatic β-cell stimulus-secretion coupling. Proc. Natl. Acad. Sci. USA 102, 17 020–17 025.
| Transthyretin constitutes a functional component in pancreatic β-cell stimulus-secretion coupling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1yksLjJ&md5=ccf52095896df3ac180477ced7c97875CAS |
Ross, R. (1999). Atherosclerosis – an inflammatory disease. N. Engl. J. Med. 340, 115–126.
| Atherosclerosis – an inflammatory disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FptFSqtQ%3D%3D&md5=133db6cec89e98f77b431daf666d74d3CAS | 9887164PubMed |
Sánchez, L. M., Chirino, A. J., and Bjorkman, P. (1999). Crystal structure of human ZAG, a fat-depleting factor related to MHC molecules. Science 283, 1914–1919.
| Crystal structure of human ZAG, a fat-depleting factor related to MHC molecules.Crossref | GoogleScholarGoogle Scholar | 10206894PubMed |
Sheehan, M. T. (2004). Polycystic ovarian syndrome: diagnosis and management. Clin. Med. Res. 2, 13–27.
| Polycystic ovarian syndrome: diagnosis and management.Crossref | GoogleScholarGoogle Scholar | 15931331PubMed |
Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850–858.
| Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XntlygtA%3D%3D&md5=e077467f1ef1f07b4cadec00fe7d5930CAS | 8779443PubMed |
Shinkai, Y., Satoh, H., Takeda, N., Fukuda, M., Chiba, E., Kato, T., Kuramochi, T., and Araki, Y. (2002). A testicular germ cell-associated serine-threonine kinase, MAK, is dispensable for sperm formation. Mol. Cell. Biol. 22, 3276–3280.
| A testicular germ cell-associated serine-threonine kinase, MAK, is dispensable for sperm formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtlWgsL0%3D&md5=61fae8ff4de0e2dadbceac3ea584fe8bCAS | 11971961PubMed |
Stan, S., Delvin, E., Lambert, M., Seidman, E., and Levy, E. (2003). ApoA-IV: an update on regulation and physiologic functions. Biochim. Biophys. Acta 1631, 177–187.
| ApoA-IV: an update on regulation and physiologic functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFaisbs%3D&md5=b74d3e59abd85f4682ab38d41c01ff63CAS | 12633684PubMed |
Stein, I. F., and Leventhal, M. L. (1935). Amenorrhea associated with bilateral polycystic ovaries. Am. J. Obstet. Gynecol. 29, 181–191.
Tso, P., Liu, M., and Kalogeris, T. J. (1999). The role of apolipoprotein A-IV in food intake regulation. J. Nutr. 129, 1503–1506.
| 1:CAS:528:DyaK1MXkslSntrY%3D&md5=ebb2e734eaa156253a284cc154bd317dCAS | 10419981PubMed |
Weiss, G., Goldsmith, L. T., Taylor, R. N., Bellet, D., and Taylor, H. S. (2009). Inflammation in reproductive disorders. Reprod. Sci. 16, 216–229.
| Inflammation in reproductive disorders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsV2hu7w%3D&md5=ba5a3ffd15c796a3558ee05b84bb6103CAS | 19208790PubMed |
Zannis, V. I., Chroni, A., and Krieger, M. (2006). Role of apoA-I, ABCA1, LCAT, and SR-BI in the biogenesis of HDL. J. Mol. Med. 84, 276–294.
| Role of apoA-I, ABCA1, LCAT, and SR-BI in the biogenesis of HDL.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVSmsL4%3D&md5=80e3939f51351dff651ce651dd436ebeCAS | 16501936PubMed |
Zhao, S., Qiao, J., Li, M., Zhang, X., Yu, J., and Li, R. (2007). Discovery of distinct protein profiles for polycystic ovary syndrome with and without insulin resistance by surface-enhanced laser adsorption/ionisation time of flight mass spectrometry. Fertil. Steril. 88, 145–151.
| Discovery of distinct protein profiles for polycystic ovary syndrome with and without insulin resistance by surface-enhanced laser adsorption/ionisation time of flight mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFGks7w%3D&md5=f56d73c7639af264b30376a89a15d3aaCAS | 17562338PubMed |
Zisman, A., Peroni, O. D., Abel, E. D., Michael, M. D., Mauvais-Jarvis, F., Lowell, B. B., Wojtaszewski, J. F., Hirshman, M. F., Virkamaki, A., Goodyear, L. J., Kahn, R., and Kahn, B. B. (2000). Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat. Med. 6, 924–928.
| Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFamtLw%3D&md5=2a639c13c770121d90b64179258ed1acCAS | 10932232PubMed |
Zorzano, A., Fandos, C., and Palacín, M. (2000). Role of plasma membrane transporters in muscle metabolism. Biochem. J. 349, 667–688.
| 1:CAS:528:DC%2BD3cXmtVWnt7s%3D&md5=e0c777dacf48d30edcb02e9de28bb81dCAS | 10903126PubMed |
