Loss of Growth arrest specific gene 6 (Gas6) results in altered GnRH neuron migration, delayed vaginal opening and sexual maturation in mice

Molecular and Cellular Endocrinology

Volumn 393, Issue 1-2, 2014, Pages 164-170

  Salian Mehta, Smita ^a   Xu, Mei ^a   Pierce, Angela ^a   Bliesner, Brian ^a   Tobet, Stuart ^c   Wierman, Margaret E ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Gas6; GnRH neurons; TAM family

Indexed keywords

AXL PROTEIN; GONADORELIN; MEMBRANE RECEPTOR; MER PROTEIN; MESSENGER RNA; TYRO3 PROTEIN; UNCLASSIFIED DRUG; GROWTH ARREST-SPECIFIC PROTEIN 6; SIGNAL PEPTIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DELAYED VAGINAL OPENING; EMBRYO; ENZYME ACTIVATION; ESTRUS CYCLE; FEMALE; FEMALE GENITAL SYSTEM; GAS6 GENE; GENE EXPRESSION; GENE LOSS; GROWTH DISORDER; MALE; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PERIKARYON; PHENOTYPE; PRIORITY JOURNAL; REPRODUCTION; SEXUAL MATURATION; UPREGULATION; ANIMAL; CELL MOTION; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; VAGINA;

ANIMALS; CELL MOVEMENT; FEMALE; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; NEURONS; REAL-TIME POLYMERASE CHAIN REACTION; SEXUAL MATURATION; VAGINA;

EID: 84904282353     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.06.015     Document Type: Article

References (35)

1. Allen M.P., Zeng C., Schneider K., Xiong X., Meintzer M.K., Bellosta P., Basilico C., Varnum B., Heidenreich K.A., Wierman M.E. Growth arrest-specific gene 6 (Gas6)/adhesion related kinase (Ark) signaling promotes gonadotropin-releasing hormone neuronal survival via extracellular signal-regulated kinase (ERK) and Akt. Mol. Endocrinol. 1999, 13:191-201.
2. Allen M.P., Xu M., Linseman D.A., Pawlowski J.E., Bokoch G.M., Heidenreich K.A., Wierman M.E. Adhesion-related kinase repression of gonadotropin-releasing hormone gene expression requires Rac activation of the extracellular signal-regulated kinase pathway. J. Biol. Chem. 2002, 277:38133-38140.
3. Bisenius E.S., Veeramachaneni D.N., Sammonds G.E., Tobet S. Sex differences and the development of the rabbit brain: effects of vinclozolin. Biol. Reprod. 2006, 75:469-476.
4. Bless E., Raitcheva D., Henion T.R., Tobet S., Schwarting G.A. Lactosamine modulates the rate of migration of GnRH neurons during mouse development. Eur. J. Neurosci. 2006, 24:654-660.
5. Cariboni A., Maggi R., Parnavelas J.G. From nose to fertility: the long migratory journey of gonadotropin-releasing hormone neurons. Trends Neurosci. 2007, 30:638-644.
6. Fernandez-Fernandez L., Bellido-Martin L., Garcia de Frutos P. Growth arrest-specific gene 6 (GAS6). An outline of its role in haemostasis and inflammation. Thromb. Haemost. 2008, 100:604-610.
7. Goruppi S., Ruaro E., Schneider C. Gas6, the ligand of Axl tyrosine kinase receptor, has mitogenic and survival activities for serum starved NIH3T3 fibroblasts. Oncogene 1996, 12:471-480.
8. Grosdemouge I., Bachelot A., Lucas A., Baran N., Kelly P.A., Binart N. Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod. Biol. Endocrinol. 2003, RB&E.1, 12.
9. Herbison A.E., Porteous R., Pape J.R., Mora J.M., Hurst P.R. Gonadotropin-releasing hormone neuron requirements for puberty, ovulation, and fertility. Endocrinology 2008, 149:597-604.
10. Hill, M.A., 2014. Embryology carnegie stage comparison. http://embryology.med.unsw.edu.au/embryology/index.php?title=Carnegie_Stage_Comparison.
11. Laurance S., Lemarie C.A., Blostein M.D. Growth arrest-specific gene 6 (gas6) and vascular hemostasis. Adv. Nutr. 2012, 3:196-203.
12. Lederman M.A., Lebesgue D., Gonzalez V.V., Shu J., Merhi Z.O., Etgen A.M., Neal-Perry G. Age-related LH surge dysfunction correlates with reduced responsiveness of hypothalamic anteroventral periventricular nucleus kisspeptin neurons to estradiol positive feedback in middle-aged rats. Neuropharmacology 2010, 58:314-320.
13. Lemke G., Rothlin C.V. Immunobiology of the TAM receptors. Nat. Rev. Immunol. 2008, 8:327-336.
14. Linger R.M., Keating A.K., Earp H.S., Graham D.K. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv. Cancer Res. 2008, 100:35-83.
15. Livne I., Gibson M.J., Silverman A.J. Biochemical differentiation and intercellular interactions of migratory gonadotropin-releasing hormone (GnRH) cells in the mouse. Dev. Biol. 1993, 159:643-656.
16. Manfioletti G., Brancolini C., Avanzi G., Schneider C. The protein encoded by a growth arrest-specific gene (gas6) is a new member of the vitamin K-dependent proteins related to protein S, a negative coregulator in the blood coagulation cascade. Mol. Cell. Biol. 1993, 13:4976-4985.
17. Matsumoto S., Yamazaki C., Masumoto K.H., Nagano M., Naito M., Soga T., Hiyama H., Matsumoto M., Takasaki J., Kamohara M., Matsuo A., Ishii H., Kobori M., Katoh M., Matsushime H., Furuichi K., Shigeyoshi Y. Abnormal development of the olfactory bulb and reproductive system in mice lacking prokineticin receptor PKR2. Proc. Natl. Acad. Sci. USA 2006, 103:4140-4145.
18. Nakano T., Kawamoto K., Higashino K., Arita H. Prevention of growth arrest-induced cell death of vascular smooth muscle cells by a product of growth arrest-specific gene, gas6. FEBS Lett. 1996, 387:78-80.
19. Pierce A., Bliesner B., Xu M., Nielsen-Preiss S., Lemke G., Tobet S., Wierman M.E. Axl and Tyro3 modulate female reproduction by influencing gonadotropin-releasing hormone neuron survival and migration. Mol. Endocrinol. 2008, 22:2481-2495.
20. Pierce A., Xu M., Bliesner B., Liu Z., Richards J., Tobet S., Wierman M.E. Hypothalamic but not pituitary or ovarian defects underlie the reproductive abnormalities in Axl/Tyro3 null mice. Mol. Cell. Endocrinol. 2011, 339:151-158.
21. Prasad D., Rothlin C.V., Burrola P., Burstyn-Cohen T., Lu Q., Garcia de Frutos P., Lemke G. TAM receptor function in the retinal pigment epithelium. Mol. Cell. Neurosci. 2006, 33:96-108.
22. Prieto A.L., Weber J.L., Tracy S., Heeb M.J., Lai C. Gas6, a ligand for the receptor protein-tyrosine kinase Tyro-3, is widely expressed in the central nervous system. Brain Res. 1999, 816:646-661.
23. Prieto A.L., Weber J.L., Lai C. Expression of the receptor protein-tyrosine kinases Tyro-3, Axl, and mer in the developing rat central nervous system. J. Comp. Neurol. 2000, 425:295-314.
24. Salian-Mehta S., Xu M., Wierman M.E. AXL and MET crosstalk to promote gonadotropin releasing hormone (GnRH) neuronal cell migration and survival. Mol. Cell. Endocrinol. 2013, 374:92-100.
25. Schneider C., King R.M., Philipson L. Genes specifically expressed at growth arrest of mammalian cells. Cell 1988, 54:787-793.
26. Schwanzel-Fukuda M., Pfaff D.W. Origin of luteinizing hormone-releasing hormone neurons. Nature 1989, 338:161-164.
27. Schwarting G.A., Henion T.R., Nugent J.D., Caplan B., Tobet S. Stromal cell-derived factor-1 (chemokine C-X-C motif ligand 12) and chemokine C-X-C motif receptor 4 are required for migration of gonadotropin-releasing hormone neurons to the forebrain. J. Neurosci. 2006, 26:6834-6840.
28. Scott R.S., McMahon E.J., Pop S.M., Reap E.A., Caricchio R., Cohen P.L., Earp H.S., Matsushima G.K. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 2001, 411:201-211.
29. Tobet S.A., Schwarting G.A. Minireview: recent progress in gonadotropin-releasing hormone neuronal migration. Endocrinology 2006, 147:1159-1165.
30. 2+ channel beta4 subunit creates a uniquely folded N-terminal protein binding domain with cell-specific expression in the cerebellar cortex. J. Neurosci. 2006, 26:2635-2644.
31. Wierman M.E., Pawlowski J.E., Allen M.P., Xu M., Linseman D.A., Nielsen-Preiss S. Molecular mechanisms of gonadotropin-releasing hormone neuronal migration. Trends Endocrinol. Metab. 2004, 15:96-102.
32. Wu H., Tang H., Chen Y., Wang H., Han D. High incidence of distal vaginal atresia in mice lacking Tyro3 RTK subfamily. Mol. Reprod. Dev. 2008, 75:1775-1782.
33. Xiong W., Chen Y., Wang H., Wu H., Lu Q., Han D. Gas6 and the Tyro 3 receptor tyrosine kinase subfamily regulate the phagocytic function of Sertoli cells. Reproduction 2008, 135:77-87.
34. Yagami T., Ueda K., Asakura K., Sakaeda T., Nakazato H., Kuroda T., Hata S., Sakaguchi G., Itoh N., Nakano T., Kambayashi Y., Tsuzuki H. Gas6 rescues cortical neurons from amyloid beta protein-induced apoptosis. Neuropharmacology 2002, 43:1289-1296.
35. Yanagita M., Ishimoto Y., Arai H., Nagai K., Ito T., Nakano T., Salant D.J., Fukatsu A., Doi T., Kita T. Essential role of Gas6 for glomerular injury in nephrotoxic nephritis. J. Clin. Investig. 2002, 110:239-246.