Endocrinology, Vol 137, 160-165, Copyright © 1996 by Endocrine Society

ARTICLES

Developmental expression of a candidate mullerian inhibiting substance type II receptor

J Teixeira, WW He, PC Shah, N Morikawa, MM Lee, EA Catlin, PL Hudson, J Wing, DT Maclaughlin and PK Donahoe
Pediatric Surgical Research Laboratory, Massachusetts General Hospital, Boston 02114, USA.

We have isolated a candidate Mullerian inhibiting substance (MIS) type II receptor complementary DNA from an embryonic rat urogenital ridge library and have studied its binding to MIS, its developmental pattern of expression and tissue distribution. By in situ hybridization with a full-length riboprobe, the receptor is expressed in the mesenchymal cells surrounding the Mullerian duct at embryonic days 14, 15, and 16 and in tubular and follicular structures of the rat fetal gonads. Expression of the messenger RNA was also seen in the granules cells and seminiferous tubules of pubertal gonads. Northern analysis revealed that the MIS type II receptor messenger RNA is highly expressed in embryonic, pubertal, and adult testes and ovaries, as well as in the gravid uterus. The timing of expression in the gonads of both sexes was also analyzed by Northern analyses that showed high levels of expression at the time of Mullerian duct regression, much lower levels neonatally and prepubertally and then increased expression again with sexual maturation. The tissue and developmental specificity of expression of this receptor, which make it likely that this is the functional MIS type II receptor, can be used to advantage in therapeutic targeting strategies and to decipher the function of MIS in the gonads.

This article has been cited by other articles:

				E. Shiraishi, N. Yoshinaga, T. Miura, H. Yokoi, Y. Wakamatsu, S.-I. Abe, and T. Kitano Mullerian Inhibiting Substance Is Required for Germ Cell Proliferation during Early Gonadal Differentiation in Medaka (Oryzias latipes) Endocrinology, April 1, 2008; 149(4): 1813 - 1819. [Abstract] [Full Text] [PDF]

				N. Renlund, R. Pieretti-Vanmarcke, F. H. O'Neill, L. Zhang, P. K. Donahoe, and J. Teixeira c-Jun N-terminal Kinase Inhibitor II (SP600125) Activates Mullerian Inhibiting Substance Type II Receptor-Mediated Signal Transduction Endocrinology, January 1, 2008; 149(1): 108 - 115. [Abstract] [Full Text] [PDF]

				J. Klattig, R. Sierig, D. Kruspe, B. Besenbeck, and C. Englert Wilms' Tumor Protein Wt1 Is an Activator of the Anti-Mullerian Hormone Receptor Gene Amhr2 Mol. Cell. Biol., June 15, 2007; 27(12): 4355 - 4364. [Abstract] [Full Text] [PDF]

				R. Pieretti-Vanmarcke, P. K. Donahoe, L. A. Pearsall, D. M. Dinulescu, D. C. Connolly, E. F. Halpern, M. V. Seiden, and D. T. MacLaughlin Mullerian Inhibiting Substance enhances subclinical doses of chemotherapeutic agents to inhibit human and mouse ovarian cancer PNAS, November 14, 2006; 103(46): 17426 - 17431. [Abstract] [Full Text] [PDF]

				T. T. Tran, D. L. Segev, V. Gupta, H. Kawakubo, G. Yeo, P. K. Donahoe, and S. Maheswaran Mullerian Inhibiting Substance Regulates Androgen-Induced Gene Expression and Growth in Prostate Cancer Cells through a Nuclear Factor-{kappa}B-Dependent Smad-Independent Mechanism Mol. Endocrinol., October 1, 2006; 20(10): 2382 - 2391. [Abstract] [Full Text] [PDF]

				Q.-a. Yuan, H. H. Simmons, M. K. Robinson, M. Russeva, W. A. Marasco, and G. P. Adams Development of engineered antibodies specific for the Mullerian inhibiting substance type II receptor: a promising candidate for targeted therapy of ovarian cancer. Mol. Cancer Ther., August 1, 2006; 5(8): 2096 - 2105. [Abstract] [Full Text] [PDF]

				Y. Zhan, A. Fujino, D. T. MacLaughlin, T. F. Manganaro, P. P. Szotek, N. A. Arango, J. Teixeira, and P. K. Donahoe Mullerian inhibiting substance regulates its receptor/SMAD signaling and causes mesenchymal transition of the coelomic epithelial cells early in Mullerian duct regression Development, June 15, 2006; 133(12): 2359 - 2369. [Abstract] [Full Text] [PDF]

				R. Pieretti-Vanmarcke, P. K. Donahoe, P. Szotek, T. Manganaro, M. K. Lorenzen, J. Lorenzen, D. C. Connolly, E. F. Halpern, and D. T. MacLaughlin Recombinant Human Mullerian Inhibiting Substance Inhibits Long-term Growth of MIS Type II Receptor-Directed Transgenic Mouse Ovarian Cancers In vivo Clin. Cancer Res., March 1, 2006; 12(5): 1593 - 1598. [Abstract] [Full Text] [PDF]

				D. Boerboom, M. Paquet, M. Hsieh, J. Liu, S. P. Jamin, R. R. Behringer, J. Sirois, M. M. Taketo, and J. S. Richards Misregulated Wnt/{beta}-Catenin Signaling Leads to Ovarian Granulosa Cell Tumor Development Cancer Res., October 15, 2005; 65(20): 9206 - 9215. [Abstract] [Full Text] [PDF]

				Y. Yin and L. Ma Development of the Mammalian Female Reproductive Tract J. Biochem., June 1, 2005; 137(6): 677 - 683. [Abstract] [Full Text] [PDF]

				V. Gupta, J. L. Carey, H. Kawakubo, A. Muzikansky, J. E. Green, P. K. Donahoe, D. T. MacLaughlin, and S. Maheswaran Mullerian inhibiting substance suppresses tumor growth in the C3(1)T antigen transgenic mouse mammary carcinoma model PNAS, March 1, 2005; 102(9): 3219 - 3224. [Abstract] [Full Text] [PDF]

				E. J. Renaud, D. T. MacLaughlin, E. Oliva, B. R. Rueda, and P. K. Donahoe Endometrial cancer is a receptor-mediated target for Mullerian Inhibiting Substance PNAS, January 4, 2005; 102(1): 111 - 116. [Abstract] [Full Text] [PDF]

				Y. Zhou, S. Scolavino, S. F. Funderburk, L. F. Ficociello, X. Zhang, and A. Klibanski Receptor Internalization-Independent Activation of Smad2 in Activin Signaling Mol. Endocrinol., July 1, 2004; 18(7): 1818 - 1826. [Abstract] [Full Text] [PDF]

				C. J. Jorgez, M. Klysik, S. P. Jamin, R. R. Behringer, and M. M. Matzuk Granulosa Cell-Specific Inactivation of Follistatin Causes Female Fertility Defects Mol. Endocrinol., April 1, 2004; 18(4): 953 - 967. [Abstract] [Full Text] [PDF]

				G. Y. Bedecarrats, F. H. O'Neill, E. R. Norwitz, U. B. Kaiser, and J. Teixeira Regulation of gonadotropin gene expression by Mullerian inhibiting substance PNAS, August 5, 2003; 100(16): 9348 - 9353. [Abstract] [Full Text] [PDF]

				A. Hossain and G. F. Saunders Synergistic Cooperation between the {beta}-Catenin Signaling Pathway and Steroidogenic Factor 1 in the Activation of the Mullerian Inhibiting Substance Type II Receptor J. Biol. Chem., July 11, 2003; 278(29): 26511 - 26516. [Abstract] [Full Text] [PDF]

				D. C. Connolly, R. Bao, A. Y. Nikitin, K. C. Stephens, T. W. Poole, X. Hua, S. S. Harris, B. C. Vanderhyden, and T. C. Hamilton Female Mice Chimeric for Expression of the Simian Virus 40 TAg under Control of the MISIIR Promoter Develop Epithelial Ovarian Cancer Cancer Res., March 15, 2003; 63(6): 1389 - 1397. [Abstract] [Full Text] [PDF]

				V. M. Laurich, A. M. Trbovich, F. H. O'Neill, C. P. Houk, P. M. Sluss, A. H. Payne, P. K. Donahoe, and J. Teixeira Mullerian Inhibiting Substance Blocks the Protein Kinase A-Induced Expression of Cytochrome P450 17{alpha}-Hydroxylase/C17-20 Lyase mRNA in a Mouse Leydig Cell Line Independent of cAMP Responsive Element Binding Protein Phosphorylation Endocrinology, September 1, 2002; 143(9): 3351 - 3360. [Abstract] [Full Text] [PDF]

				D. L. Segev, Y. Hoshiya, M. Hoshiya, T. T. Tran, J. L. Carey, A. E. Stephen, D. T. MacLaughlin, P. K. Donahoe, and S. Maheswaran Mullerian-inhibiting substance regulates NF-kappa B signaling in the prostate in vitro and in vivo PNAS, January 1, 2002; (2002) 221599298. [Abstract] [Full Text] [PDF]

				J. Teixeira, S. Maheswaran, and P. K. Donahoe Mullerian Inhibiting Substance: An Instructive Developmental Hormone with Diagnostic and Possible Therapeutic Applications Endocr. Rev., October 1, 2001; 22(5): 657 - 674. [Abstract] [Full Text] [PDF]

				J. A. Visser, R. Olaso, M. Verhoef-Post, P. Kramer, A. P. N. Themmen, and H. A. Ingraham The Serine/Threonine Transmembrane Receptor ALK2 Mediates Mullerian Inhibiting Substance Signaling Mol. Endocrinol., June 1, 2001; 15(6): 936 - 945. [Abstract] [Full Text] [PDF]

				T. R. Clarke, Y. Hoshiya, S. E. Yi, X. Liu, K. M. Lyons, and P. K. Donahoe Mullerian Inhibiting Substance Signaling Uses a Bone Morphogenetic Protein (BMP)-Like Pathway Mediated by ALK2 and Induces Smad6 Expression Mol. Endocrinol., June 1, 2001; 15(6): 946 - 959. [Abstract] [Full Text] [PDF]

				D. T. MacLaughlin, J. Teixeira, and P. K. Donahoe Perspective: Reproductive Tract Development--New Discoveries and Future Directions Endocrinology, June 1, 2001; 142(6): 2167 - 2172. [Full Text] [PDF]

				A. M. Trbovich, P. M. Sluss, V. M. Laurich, F. H. O'Neill, D. T. MacLaughlin, P. K. Donahoe, and J. Teixeira Mullerian Inhibiting Substance lowers testosterone in luteinizing hormone-stimulated rodents PNAS, March 1, 2001; (2001) 51632298. [Abstract] [Full Text]

				A. E. Stephen, P. T. Masiakos, D. L. Segev, J. P. Vacanti, P. K. Donahoe, and D. T. MacLaughlin Tissue-engineered cells producing complex recombinant proteins inhibit ovarian cancer in vivo PNAS, February 22, 2001; (2001) 51625998. [Abstract] [Full Text]

				E. A. McGee, R. Smith, N. Spears, M. W. Nachtigal, H. Ingraham, and A. J.W. Hsueh Mullerian Inhibitory Substance Induces Growth of Rat Preantral Ovarian Follicles Biol Reprod, January 1, 2001; 64(1): 293 - 298. [Abstract] [Full Text]

				S Allard, P Adin, L Gouedard, N di Clemente, N Josso, M. Orgebin-Crist, J. Picard, and F Xavier Molecular mechanisms of hormone-mediated Mullerian duct regression: involvement of beta-catenin Development, January 8, 2000; 127(15): 3349 - 3360. [Abstract] [PDF]

				J. Teixeira, D. J. Kehas, R. Antun, and P. K. Donahoe Transcriptional regulation of the rat Mullerian inhibiting substance type II receptor in rodent Leydig cells PNAS, November 23, 1999; 96(24): 13831 - 13838. [Abstract] [Full Text] [PDF]

				P. T. Masiakos, D. T. MacLaughlin, S. Maheswaran, J. Teixeira, A. F. Fuller Jr., P. C. Shah, D. J. Kehas, M. K. Kenneally, D. M. Dombkowski, T. U. Ha, et al. Human Ovarian Cancer, Cell Lines, and Primary Ascites Cells Express the Human Mullerian Inhibiting Substance (MIS) Type II Receptor, Bind, and Are Responsive to MIS Clin. Cancer Res., November 1, 1999; 5(11): 3488 - 3499. [Abstract] [Full Text] [PDF]

				J. Teixeira, E. Fynn-Thompson, A. H. Payne, and P. K. Donahoe Mullerian-Inhibiting Substance Regulates Androgen Synthesis at the Transcriptional Level Endocrinology, October 1, 1999; 140(10): 4732 - 4738. [Abstract] [Full Text]

				M. M. Lee, C. C. Seah, P. T. Masiakos, C. M. Sottas, F. I. Preffer, P. K. Donahoe, D. T. MacLaughlin, and M. P. Hardy Mullerian-Inhibiting Substance Type II Receptor Expression and Function in Purified Rat Leydig Cells Endocrinology, June 1, 1999; 140(6): 2819 - 2827. [Abstract] [Full Text]

				Y. Mishina, D. J. Whitworth, C. Racine, and R. R. Behringer High Specificity of Mullerian-Inhibiting Substance Signaling in Vivo Endocrinology, May 1, 1999; 140(5): 2084 - 2088. [Abstract] [Full Text]

				Z Gu, E. Reynolds, J Song, H Lei, A Feijen, L Yu, W He, D. MacLaughlin, J van den Eijnden-van Raaij, P. Donahoe, et al. The type I serine/threonine kinase receptor ActRIA (ALK2) is required for gastrulation of the mouse embryo Development, January 6, 1999; 126(11): 2551 - 2561. [Abstract] [PDF]

				P. d. S. Barbara, B. Moniot, F. Poulat, B. Boizet, and P. Berta Steroidogenic Factor-1 Regulates Transcription of the Human Anti-mullerian Hormone Receptor J. Biol. Chem., November 6, 1998; 273(45): 29654 - 29660. [Abstract] [Full Text] [PDF]

				C. Racine, R. Rey, M. G. Forest, F. Louis, A. Ferre, I. Huhtaniemi, N. Josso, and N. di Clemente Receptors for anti-Mullerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation PNAS, January 20, 1998; 95(2): 594 - 599. [Abstract] [Full Text] [PDF]

				C. M. HAQQ and P. K. DONAHOE Regulation of Sexual Dimorphism in Mammals Physiol Rev, January 1, 1998; 78(1): 1 - 33. [Abstract] [Full Text] [PDF]

				E. A. Catlin, V. C. Tonnu, R. G. Ebb, B. A. Pacheco, T. F. Manganaro, R. M. Ezzell, P. K. Donahoe, and J. Teixeira Mullerian Inhibiting Substance Inhibits Branching Morphogenesis and Induces Apoptosis in Fetal Rat Lung Endocrinology, February 1, 1997; 138(2): 790 - 796. [Abstract] [Full Text] [PDF]

				G Giuili, W. Shen, and H. Ingraham The nuclear receptor SF-1 mediates sexually dimorphic expression of Mullerian Inhibiting Substance, in vivo Development, January 5, 1997; 124(9): 1799 - 1807. [Abstract] [PDF]

				Y Mishina, R Rey, M J Finegold, M M Matzuk, N Josso, R L Cate, and R R Behringer Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes & Dev., October 15, 1996; 10(20): 2577 - 2587. [Abstract] [PDF]

				D. L. Segev, T. U. Ha, T. T. Tran, M. Kenneally, P. Harkin, M. Jung, D. T. MacLaughlin, P. K. Donahoe, and S. Maheswaran Mullerian Inhibiting Substance Inhibits Breast Cancer Cell Growth through an NFkappa B-mediated Pathway J. Biol. Chem., September 8, 2000; 275(37): 28371 - 28379. [Abstract] [Full Text] [PDF]

				T. U. Ha, D. L. Segev, D. Barbie, P. T. Masiakos, T. T. Tran, D. Dombkowski, M. Glander, T. R. Clarke, H. K. Lorenzo, P. K. Donahoe, et al. Mullerian Inhibiting Substance Inhibits Ovarian Cell Growth through an Rb-independent Mechanism J. Biol. Chem., November 17, 2000; 275(47): 37101 - 37109. [Abstract] [Full Text] [PDF]

				D. L. Segev, Y. Hoshiya, A. E. Stephen, M. Hoshiya, T. T. Tran, D. T. MacLaughlin, P. K. Donahoe, and S. Maheswaran Mullerian Inhibiting Substance Regulates NFkappa B Signaling and Growth of Mammary Epithelial Cells in Vivo J. Biol. Chem., July 13, 2001; 276(29): 26799 - 26806. [Abstract] [Full Text] [PDF]

				A. E. Stephen, P. T. Masiakos, D. L. Segev, J. P. Vacanti, P. K. Donahoe, and D. T. MacLaughlin Tissue-engineered cells producing complex recombinant proteins inhibit ovarian cancer in vivo PNAS, March 13, 2001; 98(6): 3214 - 3219. [Abstract] [Full Text] [PDF]

				A. M. Trbovich, P. M. Sluss, V. M. Laurich, F. H. O'Neill, D. T. MacLaughlin, P. K. Donahoe, and J. Teixeira Mullerian Inhibiting Substance lowers testosterone in luteinizing hormone-stimulated rodents PNAS, March 13, 2001; 98(6): 3393 - 3397. [Abstract] [Full Text] [PDF]

				D. L. Segev, Y. Hoshiya, M. Hoshiya, T. T. Tran, J. L. Carey, A. E. Stephen, D. T. MacLaughlin, P. K. Donahoe, and S. Maheswaran Mullerian-inhibiting substance regulates NF-kappa B signaling in the prostate in vitro and in vivo PNAS, January 8, 2002; 99(1): 239 - 244. [Abstract] [Full Text] [PDF]