Reproductive Health and Toxicology Lab



Li Y, Adur MK, Kannan A, Davila J, Zhao Y, Nowak RA, Bagchi MK, Bagchi IC, Li Q. Progesterone alleviates endometriosis via inhibition of uterine cell proliferation, inflammation and angiogenesis in an immunocompetent mouse model. PLoS One 2016 Oct. 24;11(10):e0165347. Doi: 10.1371/journal.pone.0165347.

Koohestani F, Qiang W, MacNeill AL, Druschitz SA, Serna VA, Adur M, Kurita T, Nowak RA. Halofuginone suppresses growth of human uterine leiomyoma cells in a mouse xenograft model. Hum. Reprod. 2016; 31(7):1540-1551.

Burnett LA, Nowak RA. Exosomes mediate embryo and maternal interactions in implantation and during pregnancy. Front Biosci (Schol Ed). 2016 Jan 1;8:79-96, [Epub December 2015].

Newell-Fugate AE, Taibl JN, Alloosh M, Sturek M, Bahr JM, Nowak RA, Krisher RL. Effects of obesity and metabolic syndrome on steroidogenesis and folliculogenesis in the female Ossabaw mini-pig. PLoS One 2015; 10(6)e0128749.doi:10.1371.

Mauris J, Dieckow J, Schob S, puli B, hatton MP, Jeong, S, Bauskar A, Gbison E, Nowak R, Argueso P. Loss of CD147 results in impaired epithelial cell differentiation and malformation of the meibomian gland. Cell Death Dis 2015; Apri 16;6:e1726. Doi:10.1038.

Erbach GT, Biggers JD, Manning PC, Nowak RA. Localization of parathyroid hormone-related protein in the preimplantation mouse embryo is associated with events of blastocyst hatching. J Assist Reprod Genet 2013; 30:1009-1015.

Schiene-Fishcer C, Malesevic M, Gutknecht D, Prell E, Klein C, Nowak RA, Simon JC, Saalbach A. Anti-inflammatory effects of extracellular cyclosporins are exclusively mediated by CD147. J Med Chem 2013; 56:7302-7311 [Epub Sep 12, 2013].

Koohestani F, Braundmeier AG, Mahdian A, Seo J, Bi J, Nowak RA. Extracellular matrix collagen alters cell proliferation and cell cycle progression of human uterine leiomyoma smooth muscle cells. PLosOne 2013; 8:e75844, PMID24040420.

Nowak RA. Adiponectin to the rescue: how the embryo maintains glucose uptake in a diabetic mother. Endocrinology 2013; 154:2260-2262.

Bi J, Li Y, Sun F, Saalbach A, Klein C, Miller DJ, Hess R, Nowak RA. Basigin null mutant male mice are sterile and exhibit impaired interactions between germ cells and Sertoli cells. Dev Biol 2013; 380:145-156 [Epub May 30, 2013].

Varghese BV, Koohestani F, McWilliams C, Gunewardena S, Kinsey WH, Nowak RA, Nothnick WB, Chennathukuzhi VM. Loss of the repressor REST in uterine fibroids promotes aberrant G protein-coupled receptor 10 expression and activates mammalian target of rapamycin pathway. Proc Natl Acad Sci USA 2013; 110:2187-2192 [ Epub Jan. 2, PMID23284171].

Mesquita FS, Machado SA, Drnevich J, Borowicz P, Wang Z, Nowak RA. Influence of cloning by chromatin transfer on placental gene expression at Day 45 of pregnancy in cattle. Anim Reprod Sci 2013; 136:231-244 [Epub 2012 Nov 8].

Lessey BA, Nagarkatti M, Zhou J, Young SL, Adur MK, Nowak RA. Peripheral and local cytokines including IL-8, IL-9 and IL-17 are elevated in endometriosis: an in vivo and in vitro analysis before and after surgery suggests a mechanism for endometrial dysfunction. Fertil Steril 2012; 98:S92-93.

Burnett LA, Light MM, Nowak RA. Stimulation of GPR30 increases release of EMMPRIN-containing microvesicles in human uterine epithelial cells. J Clin Endocrinol Metab 2012;87:4613-4622 [Epub 2012 Sep 25].

Machado SA, Bahr JM, Hales DB, Braundmeier AG, Quade BJ, Nowak RA. Validation of the aging hen as an animal model for uterine leiomyomas. Biol Reprod 2012; 87:86,1-11 [Epub 2012 Jul 18].

Fitzgerald JB, Chennathukuzhi V, Koohestani F, Nowak RA, Christenson LK. Role of microRNA-21 and prgrammed cell death 4 in the pathogenesis of human uterine leiomyomas. Fertil Steril 2012, 98:726-734 [Epub Jun 22].

Braundmeier AG, Dayger CA, Mehrotra P, Belton Jr. RJ, Nowak RA. EMMPRIN is secreted by human uterine epithelial cells in microvesicles and stimulates metalloproteinase production by human uterine fibroblast cells. Reproductive Sciences 2012; 19:1292-1301, [Epub Jun 22, 2012].

Braundmeier AG, Jackson K, Hastings J, Koehler J, Nowak RA, Fazleabas A. Endometriosis alters the peripheral and endometrial regulatory T cell population in the non-human primate. Human Reproduction 2012; 27:1712-1722, [Epub March 22, 2012].

Seizer P, Ochmann C, Schonberger T, Zach S, Lengerke C, Rose M, Klingel K, Kandolf R, MacDonald HR, Nowak RA, Engelhardt S, Gawaz M, May AE. Disrupting the EMMPRIN (CD147)-Cyclophilin A interaction reduces infarct size and preserves systolic function after myocardial ischemia and reperfusion. Arteriosclerosis, Thrombosis, and Vascular Biology, 2011 ;31:1377-1386 [Epub March 24, 2011].

Marsh EE, Wu J, Cardozo E, Nowak R, Bulun SE, Veis A. A vitamin A day: the role of vitamin C (ascorbic acid) and ITS transporters in the transcription and secretion of COL1A1 and COL1A2 in leiomyoma and myometrium. Fert Steril 2010, 90:S141-142.

Braundmeier AG, Fazleabas AT, Nowak RA. Extracellular matrix metalloproteinase inducer (EMMPRIN) expression in baboon endometrium: menstrual cycle and endometriosis. Reproduction 2010;140;911-920 [Epub September 14, 2010].

Chen L, Bi J, Nakai M, Bunick D, Couse J, Korach KS, Nowak RA. Expression of basigin in reproductive tissues of estrogen receptor-α or –β null mice. Reproduction 2010;139:1057-1066, [Epub April 13, 2010].

Mesquita FS, Dyer SN, Heinrich DA, Bulun SE, Marsh EE, Nowak RA. Reactive oxygen species mediate mitogenic growth factor signaling pathways in human leiomyoma smooth muscle cells. Biology of Reproduction 2010; 82:341-351 [Epub September 9, 2009].

Grudzien MM, Low P, Manning PC, Arredondo M, Belton Jr. RJ, Nowak RA. The antifibrotic drug halofuginone inhibits proliferation and collagen production by human leiomyoma and myometrial smooth muscle cells. Fertility and Sterility 2010; 93: 1290-1298, [Epub January 8, 2009].

Chen L, Belton Jr. RJ, Nowak RA. Basigin mediated gene expression changes in mouse uterine stromal cells during implantation. Endocrinology 2009, 150(2):966-976, [Epub October 1, 2008].

Belton Jr. RJ, Chen L, Mesquita FS, Nowak RA. Basigin-2 is a cell surface receptor for soluble basigin ligand. Journal of Biological Chemistry 2008; 283:17805-17814. [Epub April 22, 2008].

Albin DM, Wubben JE, Rowlett JM, Tappenden KA, Nowak RA. Small intestinal transport and barrier function respond differently to acute immune challenge in two porcine breeds. Journal of Animal Science, 2007; 85:2517-2523. [Epub May 25, 2007].

Chen L, Nakai M, Belton Jr. R J, and Nowak RA. Expression of extracellular matrix metalloproteinase inducer and matrix metalloproteinases during mouse embryonic development. Reproduction 2007;133:405-414.

Braundmeier A and Nowak RA. Cytokines regulate matrix metalloproteinase production in human endometrial stromal cells. American Journal of Reproductive Immunology 2006:56:201-214.

Braundmeier A, Fazleabas A, Lessey BA, Guo F, Toole BP, Nowak RA. Extra-cellular matrix metalloproteinase inducer (EMMPRIN) regulates metalloproteinases in the human endometrium. Journal of Clinical Endocrinology and Metabolism 2006;91:2358-65 [Epub March 7, 2006].

Nakai M, Chen L and Nowak RA. Tissue distribution of basigin and monocarboxylate transporter I in the adult male mouse: a study using the wild type and basigin gene knockout mice. The Anatomical Record Part A 2006;288A:527-535.

Nowak RA. Drug therapies for uterine fibroids: a new approach to an old problem. Drug Discovery Today: Therapeutic Strategies 2004;1(2):237-242.

Mason HR, Lake AC, Wubben JE, Nowak RA, Castellot JJ Jr. The growth arrest-specific gene CCN5 is deficient in human leiomyomas and inhibits the proliferation and motility of cultured human uterine smooth muscle cells. Molecular Human Reproduction 2004;10:181-187, [Epub January 29, 2004].

Mason HR, Grove-Strawser D, Rubin BS, Nowak RA, Castellot JJ Jr. Estrogen induces CCN5 expression in the rat uterus in vivo. Endocrinology 2004;145:976-982. [Epub November 06, 2003].

Gross K.L., Neskey D.M., Manchanda N., Weremowicz S., Kleinman M., Nowak R.A., Ligon, A.H., Rogalla P., Drechsler K., Bullerdiek J., Morton C.C. HMGA2 expression in uterine leiomyomata and myometrium: Quantitative analysis and tissue culture studies. Genes, Chromosomes and Cancer 2003;38:68-79.

Mason, H., Nowak, R.A.,Morton, C.C., Castellot, J. Heparin inhibits the proliferation and motility of human uterine myometrial and leiomyoma smooth muscle cells. American Journal of Pathology 2003;162:1895-1904.

Propst, A.M., Quade, B.J., Nowak, R.A., Stewart, E.A. Granulocyte macrophage colony stimulating factor expression in adenomyosis and autologous endometrium. Journal of the Society for Gynecological Investigation 2002;9:93-97.

Propst, A.M., Quade, B.J., Gargiulo, A.R., Nowak, R.A., Stewart, E.A. Adenomyosis demonstrates increased expression of the basic fibroblast growth factor receptor/ligand system compared to autologous endometrium. Menopause 2001;8:368-371.

Lee, B. S. and Nowak, R.A. Human leiomyoma smooth muscle cells show increased expression of transforming growth factor-3 (TGF) and altered responses to the anti-proliferative effects of TGF. Journal of Clinical Endocrinology & Metabolism 2001;86:913-920.

Nowak, R.A. Novel therapeutic strategies for leiomyomas: targeting growth factors and their receptors. Environmental Health Perspectives 2000;44(vol 2):327-334.

Nowak, R.A. Fibroids: Pathophysiology and current medical treatment. In: Smith, SK (ed) Bailliere’s Clinical Obstetrics & Gynecology 1999;13(2):223-238.

Nowak, R.A., Mora, S., Diehl, T., Stewart, E.A. Prolactin is an autocrine or paracrine growth factor for human myometrial and leiomyoma cells. Gynecological and Obstetric Investigation 1999;48:127-132.

Gattas, G.J.F., Quade, B.J., Nowak, R.A., Morton, C.C. HMGI-C expression in human adult and fetal tissues and in uterine leiomyomata. Genes, Chromosomes and Cancer 1999;25:316-322.

Austin, D.J., Jain, P., Nowak, R.A., Stewart, E.A. Onapristone suppresses prolactin production in explant cultures of leiomyoma. Gynecological and Obstetric Investigation 1999;47:268-271.

Stewart, E.A., Sahakian, M., Rhoades, A., Van Voorhis, B.J., Nowak, R.A. Messenger ribonucleic acid for the gonadal luteinizing hormone/human chorionic gonadotropin receptor is not present in human endometrium. Fertility and Sterility 1999;71:368-72.

Nowak, R.A., Haimovici, F., Biggers, J.D., Erbach, G.T. Transforming growth factor- stimulates mouse blastocyst outgrowth through a mechanism involving parathyroid hormone-related protein (PTHrP). Biology of Reproduction 1999;60:85-93.

Lee, B.S., Stewart, E.A., Sahakian, M., Nowak, R.A. Interferon- is a potent inhibitor of basic fibroblast growth factor-stimulated cell proliferation in human uterine cells. American Journal of Reproductive Immunology 1998;40:19-25.

Palmer, S.S., Haynes-Johnson, D., McDermott, L., Campen, C., Diehl, T., Nowak, R.A. Increased expression of stromelysin 3 mRNA in leiomyomas (uterine fibroids) compared to myometrium. Journal of the Society for Gynecological Investigation 1998;5:203-209.

Stewart, E.A., Rhoades, A.R., Nowak, R.A. Leuprolide acetate treated leiomyomas retain their relative overexpression of collagen type I and collagen type III messenger RNAs. Journal of the Society for Gynecological Investigation 1998;5;44-47.

Lee, B.S., Margolin, S.B., Nowak, R.A. Pirfenidone: A novel pharmacological agent that inhibits leiomyoma cell proliferation and collagen production. Journal of Clinical Endocrinology and Metabolism 1998;83:219-223.

Stewart, E.A. and Nowak, R.A. New concepts in the treatment of uterine leiomyomas. Obstetrics & Gynecology 1998;92:624-627.

Anania, C.A., Stewart, E.A., Quade, B.A., Hill, J.A., Nowak, R.A. Expression of the fibroblast growth factor receptor in women with leiomyomas and abnormal uterine bleeding. Molecular Human Reproduction 1997;3:685-691.

Ishikawa, M., Elenius, K. Klagsbrun, M., Nowak , R.A. Human myometrial and leiomyoma cells show differential responsivenss to HER-1 mediated cell proliferation. J. Soc. Gynecol. Invest. 1996; 3:335-336.

Stewart, E.A. and Nowak, R.A. Leiomyoma-related bleeding: a classic hypothesis updated for the molecular era. Human Reproduction Update 1996;2:295-306.

Stewart, E.A., Austin, D.J., Jain, P., Penglase, M.D., Nowak, R.A. RU486 suppresses prolactin production in explant cultures of leiomyomas and myometrium. Fertil. Steril. 1996;65:1119-1124.

Nowak, R.A. and Friedman, A.J. The cellular and molecular physiology of uterine leiomyomas. Contemp. Obstet. Gynecol. 1995;40(5):91-102.

Stewart, E.A., Floor, A.E., Jain, P., Nowak, R.A. Relative overexpression of messenger RNA for collagen types I and III and fibronectin in myometrium of pregnancy. Obstet. and Gynecol. 1995;86:417-422.

Stewart, E.A., Jain, P., Penglase, M.D., Friedman, A.J., Nowak, R.A. The myometrium of postmenopausal women produces prolactin in response to human chorionic gonadotropin and alpha-subunit in vitro. Fertil. Steril. 1995;64:972-976.

Mangrulkar, R.S., Ono, M., Ishikawa, M., Takashima, S., Klagsbrun, M., Nowak, R.A. The isolation and characterization of heparin-binding growth factors in human leiomyomas and normal myometrium. Biol. Reprod. 1995;53:636-646.

Mashal, R.D., Fejzo, M.L.S., Friedman, A.J., Mitchner, N., Nowak, R.A., Rein, M.S., Morton, C.C., Sklar, J. Analysis of androgen receptor DNA reveals the independent clonal origins of uterine leiomyomata and the secondary nature of cytogenetic aberrations in leiomyomata development. Genes, Chromosomes, and Cancer 1994;11:1-16.

Stewart, E.A., Friedman, A.J., Peck, K., Nowak, R.A. Relative overexpression of collagen I and collagen III mRNAs by uterine leiomyomas during the proliferative phase of the menstrual cycle. J. Clin. Endo. Metab. 1994;79:900-906.

Weir, E.C., Goad, D.L., Daifotis, A.G., Burtis, W.J., Dreyer, B.E., Nowak, R.A. Relative overexpression of the parathyroid hormone-related peptide gene in human leiomyomas. J. Clin. Endo. Metab. 1994;78:784-789.

Stewart, E.A., Rein, M.S., Friedman, A.J., Nowak, R.A. Glycoprotein hormones and their common alpha-subunit stimulate prolactin production by explant cultures of human leiomyomata and myometrium. Am. J. Obstet. Gynecol. 1994;170:677-683.

Nowak, R.A., Rein, M.S., Heffner, L.J., Friedman, A.J., Tashjian, Jr., A.H. Production of prolactin by smooth muscle cells cultured from human uterine fibroid tumors. J. Clin. Endo. Metab. 1993;76:1308-1313.

Rein, M.S. and Nowak, R.A. Biology of uterine myomas an myometrium in vitro. In: Barbieri, RL (ed), Seminars in Reproductive Endocrinology 1992;10:310-319.

Yeh, J., Rein, M.S., Nowak, R.A. Presence of messenger ribonucleic acid for epidermal growth factor (EGF) and EGF receptor demonstrable in monolayer cell cultures of myometria and leiomyomata. Fertil. Steril. 1991;56:997-1000.

Nowak, R.A., Morrison, N.E., Goad, D.L., Gaffney, E.V., Tashjian, Jr., A.H. Squamous cell carcinomas often produce more than a single bone resorption-stimulating factor: Role of interleukin-1a. Endocrinology 1990;127:3061-3069.

Nowak, R.A., Wang, M.W., Hamon, M., Lamb, D., Bullock D., Heap, R.B. Effect of passive immunization against progesterone on its distribution in circulation and tissues of mice. J. Reprod. Fert. 1990;89:67l-679.

Nowak, R.A., Wang, M.W., Heap, R.B. The antifertility effect of passive immunization against progesterone is influenced by genetic factors other than H-2 haplotype. J. Endocr. 1990;l25:257-262.

Nowak, R.A., Samaras, S.E., Chorney, M.C., Hagen, D.R., Dziuk, P.J. Effect of severing the spinal cord of fetal lambs on length of gestation. Am. J. Obstet. Gynecol. 1987;l57:464-467.

Nowak, R.A. and Bahr, J.M. Secretion of a gonadotropin releasing hormone (GnRH)-like factor by the rabbit fetal placenta in vitro. Placenta 1987;8:299-304.

Ritzhaupt, L.K., Nowak, R.A., Calvo, F.O., Khan, I., Bahr, J.M. Adenylyl cyclase activity in the corpus luteum of cycling gilts. J. Reprod. Fert. 1986;78:36l-366.

Nowak, R.A., Klein, J., Pulido, D.M., Bahr, J.M. Bilateral maintenance of rabbit corpora lutea by the fetal placental unit. J. Endocr. 1986;l09:l07-ll0.

Nowak, R.A., Wiseman, B.S., Bahr, J.M. Identification of a GnRH-like factor in the rabbit fetal placenta. Biol. Reprod. 1984;3l:67-75.

Nowak, R.A. and Bahr, J.M. Maternal recognition of pregnancy in the rabbit. J. Reprod. Fert. 1983;69:623-627.

Nowak, R.A. and Bahr, J.M. Effect of embryo removal on concentrations of progesterone and LH in the rabbit. J. Reprod. Fert. 1983;68:395-399.

Scheffrahn, N.S., Wiseman, B.S., Nowak, R.A., Kesler, D.J. Induction of male sex behavior in ewes with silastic implants containing testosterone propionate. Theriogenology 1982;l8:l-l5.

Scheffrahn, N.S., Nowak, R.A., Kesler, D.J. Male sex behavior and testosterone concentrations in gilts administered testosterone propionate. Theriogenology 1981;l6:295-302.

Book Chapters: 

Nowak RA, Bi J, Koohestani F, Mesquita FS, Erbach GT.  Uterine Tumors and the Environment.  In: Comprehensive Toxicology, 3rd edition, ed. by CA McQueen, Section IV Female Reproductive Toxicology- Female Reproductive C, Elsevier, 2016; in press.   

Nowak RA, Koohestani F, Bi J, Mehrotra P, Mesquita FS, Masoud F, Machado SM.  Uterine Tumors and the Environment.  In: Comprehensive Toxicology,  2nd edition, ed. by CA McQueen, Section IV Female Reproductive Toxicology- Female Reproductive C, Elsevier, 2010;499-522.  

Nowak, R.A.  The pathophysiology of dysfunctional uterine bleeding.  In:  eds John Aplin, Asgerally Fazleabas, Stanley Glasser and Linda Giudice, The Endometrium:Molecular, Cellular and Clinical Perspectives, 2nd Edition, Informa Health Care, 2008;711-726.

Nowak, R.A.  Biological factors influencing fibroid growth: hormones and cytokines.  In: Ginsburg E (eds) Infertility and Reproductive Medicine Clinics of North America: Fibroids- Epidemiology, Biology and Treatment; Philadelphia, PA: Saunders and Co., 2002; 303-313.

Nowak, R.A.  Identification of new therapies for leiomyomas: what in vitro studies can tell us.  In: Van Voorhis B (eds) Clinical Obstetrics and Gynecology: Management Options for Uterine Fibroids; Philadelphia, PA: Lipincott and Williams, 2001;327-334.

Nowak, R.A.  Effects of growth factors on leiomyomas.  In: Osteen K and Diamond M (eds) Endometrium and Endometriosis; Malden, MA: Blackwell Science, 1997;301-310.

Nowak, R.A.  A gonadotropin releasing hormone-like factor in the rabbit placenta.  In: F. Ellendorf and E. Koch (eds) Early Pregnancy Factors, Ithaca, NY: Perinatology Press, 1985:157-159.

Conference Proceedings:

Nowak, RA.  Regulation of extra-cellular matrix in leiomyomas: a cellular and molecular approach.  In: Proceedings of the VIIth International Conference on the Extracellular Matrix of the Female Reproductive Tract and Simpson Symposia, Number 13-2004, pp 42-43.

Nowak, RA.   Sex steroid hormone action in cultured uterine myometrial cells.  Kuramoto H and Gurpide E (eds) In: Proceedings of the 1st International Symposium of the Japanese Tissue Culture Association, Churchill Livingstone; 1996;264-275.

Heap, RB, Davis, AJ, Fleet, IR, Goode, JA, Hamon, M, Nowak, RA, Stewart, HJ, Whyte, A, Flint, APF.  Maternal recognition of pregnancy.  Proceedings of the 11th International Congress on Animal Reproduction and Artificial Insemination. Dublin, Ireland, June 1988;55-60.

Heap, RB, Taussig MJ, Nowak, RA, Deverson, EV, Ellis, ST, Rider, V, Wang, MW, Feinstein, A.  Action of antiprogesterone monoclonal antibody in blocking early pregnancy.  C. Pholpramool and R. Sudsuang (eds.) In: Proceedings of the First International Congress of the Asian and Oceanian Physiological Societies; 1987;201-210.

Jarrell, V., Nowak, R.A., Bahr, J.M.  Reproduction in Rabbits. In: Proceedings of the First Annual Rabbit Industry Conference, University of Illinois, 1983; 14-20.